Significance of Genetic, Environmental, and Pre- and Postharvest

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Significance of genetic, environmental, and pre- and postharvest factors affecting carotenoid contents in crops: A review Ramesh Kumar Saini, and Young Soo Keum J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.8b01613 • Publication Date (Web): 10 May 2018 Downloaded from http://pubs.acs.org on May 15, 2018

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Journal of Agricultural and Food Chemistry

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Significance of genetic, environmental, and pre- and post-harvest factors

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affecting carotenoid contents in crops: A review

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Ramesh Kumar Saini*, Young-Soo Keum

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*Corresponding author: Tel.: þ82-2450-3739; fax: þ8234365439. [email protected]

Department of Crop Science, Konkuk University, Seoul 143-701, Republic of Korea

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ACS Paragon Plus Environment


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Abstract

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Carotenoids are a diverse group of tetraterpenoid pigments that play indispensable roles in

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plants and animals. The biosynthesis of carotenoids in plants is strictly regulated at the

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transcriptional and post-transcriptional levels in accordance with inherited genetic signals,

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developmental requirements, and in response to external environmental stimulants. The

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alteration in the biosynthesis of carotenoids under the influence of external environmental

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stimulants, such as high light, drought, salinity, and chilling stresses, has been shown to

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significantly influence the nutritional value of crop plants. In addition to these stimulants,

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several pre- and post-harvesting cultivation practices significantly influence the carotenoid

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composition and contents. Thus, this review discusses how various environmental stimulants

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and pre- and post-harvesting factors can be positively modulated for the enhanced

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biosynthesis and accumulation of carotenoids in the edible parts of crop plants, such as leaves,

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roots, tubers, flowers, fruit, and seeds. In addition, future research directions in this context

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are identified.

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Keywords: Photosynthetic pigments, abiotic stress, storage, processing, UV-C hormesis

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Introduction

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Carotenoids are a diverse group of tetraterpenoid pigments that are produced by plants and

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algae, as well as several bacteria and fungi. Carotenoids play an essential role in plant

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development, photomorphogenesis, photosynthesis, root-mycorrhizal interactions, pollination,

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seed dispersal, and the production of phytohormones, including abscisic acid (ABA),

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strigolactone (SL), and dihydroactinidiolide (DHA), and various other volatiles and signaling

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apocarotenoids.1 Carotenoids and their enzymatic (by carotenoid cleavage dioxygenases;

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CCDs) or oxidative cleavage (via singlet oxygen 1O2 attack) products called apocarotenoids

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are crucial for the growth and development of plants, comprising the assembly of

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photosystems and light harvesting complexes (LHCs) for photosynthesis and photoprotection,

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and increased tolerance to photooxidative stress. The production of signaling apocarotenoids,

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β-cyclocitral, and DHA under photooxidative stress in photosynthetic apparatus has recently

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been explored; their production induces the gene expressions that lead to an acclimation to

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stress conditions.2,3 Thus, in recent years, apocarotenoids signaling, especially by ABA, SL,

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and DHA, has been implicated in the functional interactions of plants with their changing

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environment of biotic and abiotic stress.2,4

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Similar to plants, carotenoids are important for the normal health and behavior of

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animals. Carotenoids play key roles in the following ways: 1) pigmentation of the tissues of

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some marine animals (e.g., salmon, shrimp, and lobster) and birds (e.g., flamingo, quail, and

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canary), improving their immune system, and in many cases, providing a sexual selective

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advantage; 2) carotenoid DHA is an active compound of insect pheromones, and plays a key

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role in sensing, signalling, and bio-communication; 3) improving immune function (cell-

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mediated and humoral) through their ability to enhance membrane fluidity, and gap-junction

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communications; 4) carotenoids with unsubstituted β-ionone rings (including β-Carotene: β3



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Car, α-carotene: α-Car, β-cryptoxanthin: β-Cry and γ-carotene) serve as precursors for the

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synthesis of retinol (vitamin A), retinal (key visual pigment), and retinoic acid, which

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controls neuronal differentiation and organogenesis; and 5) functioning as potent

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antioxidants, as well as delaying the progression of cardiovascular diseases, certain cancers

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(including neck, prostate, and breast), and age-related macular degeneration (AMD) of the

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eye.5–8

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Almost no animals synthesize carotenoids (except for some species of pea aphids,

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spider mites, and gall midges),9 thus relying on their daily diet to obtain these compounds. In

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a plant-based diet, carotenoid-rich green leafy vegetables, colored fruit, and carrot taproots

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principally serve as a source of carotenoids. However, the contents of carotenoids differ

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significantly among species and within species, because of the strictly controlled biosynthesis

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and accumulation. The biosynthesis of carotenoids in plants is regulated throughout the life

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cycle, starting from seed germination to seed maturation. Dynamic changes in the

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composition

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photomorphogenesis, photosynthesis, and in response to external environmental stimulants.

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The genetic, environmental, and developmental factors regulating the carotenoid biosynthetic

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pathway have been elucidated at the molecular level.1 The metabolic engineering of

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carotenogenesis has proven to be successful, and offers the potential to enhance accumulation

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in genetically modified organisms (GMO) (not discussed in this review); Golden rice is the

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most prominent example. Likewise, the positive regulation of carotenoid biosynthesis has

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served as a potential tool to improve the nutritional characteristics of high yield commercially

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grown non-GMO crops,10–14 which is critically important in addressing food security in the

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face of malnutrition. Thus, this review discusses how various environmental stimulants and

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pre-harvesting and post-harvesting factors can be positively modulated for the enhanced

of

carotenoids

occur

according

to

4


developmental

requirements,

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biosynthesis and accumulation of carotenoid in the edible parts of crop plants. The discussion

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highlights the concept of biotic and abiotic stress signals that may be involved in the

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enhanced accumulation of carotenoids and other defense-related compounds. We propose a

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concrete model of the pre-harvesting and post-harvesting factors for the positive regulation of

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carotenoid biosynthesis and accumulation in crop plants. Post-harvesting storage and

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processing are discussed to develop a comprehensive model, from crop cultivation to the

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serving of food on a plate.

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Carotenoid biosynthesis and its regulation by environmental factors

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Carotenoids are biosynthesized from the plastid-localized 2-C-methyl-D-erythritol 4-

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phosphate (MEP) pathway, leading to the synthesis of geranylgeranyl diphosphate (GGPP)

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(Fig. 1). This initial step MEP pathway is catalyzed by 1-deoxyxylulose-5-phosphate

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synthase (DXS) and 1-deoxy-D-xylulose 5-phosphate reductoisomerase (DXR).1 These are

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the key enzymes that provide sufficient flux of carotenoid precursors for enhanced

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biosynthesis.1 In the downstream pathway, the condensation of two GGPPs (C20) by

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phytoene synthase (PSY) forms phytoene (C40) as a 15-Z isomer, the first carotenoid.

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Carotenoid biosynthesis bifurcates after lycopene (LYC) to produce epsilon (ε)- (e.g., α-Car)

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and beta (β)-carotenoids (e.g., β-Car) by the enzymatic activities of LYC-ε-cyclase (CLY-ε)

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and LYC-β-cyclase (LCY-β), respectively. A molecular synergism between these two

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cyclases plays a significant regulatory role as the major determinant of flux through the

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branch, leading to the production of α-Car and lutein (Lut) on one side, and β-Car, zeaxanthin

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(Zea), violaxanthin (Vio), and neoxanthin (Neo) on the other side (Fig. 1).1

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Elucidation of the carotenoid biosynthesis regulation has revealed several processes

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that are strongly modulated by epigenetic factors, environmental conditions, and their 5



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interactions.1 Thus, the environmental conditions during crop cultivation have been

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considered as the potential targets for improving the composition and contents of

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carotenoids.15 Figure 1 shows that light is the major signal regulating carotenoid biosynthesis

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in plants, while phytochromes, a class of photoreceptor, transduce these light signals.

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Phytochromes are present in two photoreversible forms, Pr and Pfr, which function as a

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receiver of red (R; (650–670) nm) and far-red (FR; (705–740) nm) regions of visible light,

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respectively. In a dark condition, the Pr form absorbs R light, and is converted to the

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biologically active Pfr form, which interacts with signaling components that eventually

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translate the light signal into physiological responses by altering the gene expression.16 In

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recent years, phytochrome-interacting factor 1 (PIF1; a negative regulator of carotenoid

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biosynthesis) and other transcription factors of the phytochrome-interacting factor (PIF) have

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been reported.11,17 In dark-grown seedlings, PIF1 and other PIFs bind to the promoter of PSY,

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the key rate-limiting enzyme of the pathway, and repress its transcription, resulting in a

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decrease in the accumulation of carotenoids (Fig. 2(a)). In contrast, the photoactivated

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phytochromes mediated light signals trigger the degradation of PIFs during de-etiolation,

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which allows a prompt derepression of PSY gene expression, thus enhancing the

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accumulation of carotenoids.17 The long hypocotyl 5 (HY5) transcription factor, a potent PIFs

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antagonist, has also recently been identified, and is required for the light induction of PSY

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expression and carotenoid biosynthesis in response to light at a cooler ambient temperature

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(e.g., 17 °C).18

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Light positively regulates carotenoid biosynthesis, other than a few exceptions such

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as the significant decrease in the total carotenoid contents in the illuminated roots of colored

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carrot.11 The orange and yellow carrot taproots accumulate excessive amounts of provitamin

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A carotenoids (α- and β-Car) as large crystals inside chromoplasts that develop from 6


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carotenoid-devoid leucoplasts. Interestingly, when these roots are exposed to light,

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chromoplast-containing carotenoids can differentiate into chloroplasts (redifferentiation of

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chromoplasts into chloroplasts), resulting in a decrease in the amount of carotenoids (Fig.

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2(b)). The acute mechanism of massive carotenoid accumulation in carrot taproots is mostly

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unknown. However, with the help of the genome-wide assembly of different colored carrots,

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a candidate gene, DCAR_032551, has recently been identified that is co-expressed with light-

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inducible isoprenoid pathway genes, including DXS1, CLY-ε, and HY5.10 Interestingly, the

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DCAR_032551 gene products showed homology with the A. thaliana PSEUDO-

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ETIOLATION IN LIGHT (PEL) protein, which shows inadequate responses to light

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(etiolated phenotype). These mutants cannot inhibit the light-induced changes in the

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transcriptome associated with de-etiolation and photomorphogenesis in non-photosynthetic

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tissues such as roots. Based on this evidence, it is believed that DCAR_032551 regulates

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upstream photosystem development and functional processes, including photomorphogenesis

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and root de-etiolation, resulting in massive carotenoid accumulation in the carrot.

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The metabolome of tomato fruits, especially carotenoid accumulation during fruit

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ripening, is also significantly influenced by light. The ripening of tomato and many other

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fleshy fruits is associated with the differentiation of green fruit chloroplasts into ripe fruit

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chromoplasts.11 The characteristic orange and red colors of ripe tomatoes results from the

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degradation of chlorophylls (Chl) and the accumulation of carotenoids, particularly LYC and

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β-Car. Among several elucidated mechanisms of tomato fruit ripening, the crucial role of the

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phytochrome-induced degradation of PIF has recently been explored.19 In mature green

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tomato fruit, PIF1 homolog (PIF1a) directly binds to the PBE box of the PSY1 promoter to

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repress carotenogenesis. On the other hand, during tomato fruit ripening (Fig 2(c)), strict

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developmentally-controlled degradation of Chl reduces the self-shading effect, hence 7



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allowing the phytochrome-mediated degradation of PIF1. Consequently, PSY1 is de-

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repressed, which boosts carotenoids biosynthesis and shifts the carotenoid composition from

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leaf-like xanthophylls (mainly Lut, Neo, and β-Car) to carotenes (mainly LYC and β-Car).11

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In addition to light, a large number of biotic (e.g., colonization of plant root with

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arbuscular mycorrhizal (AM) fungi, as well as viral, bacterial, fungal, and herbivore

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infection) and abiotic factors (e.g., soil salinity, drought, temperature, and nutrient

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availability) influence the availability of isoprenoid precursors by altering the expression of

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nearly all the MEP pathway genes, which significantly influences the downstream pathways

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of carotenoids biosynthesis.1 Moreover, all these factors at moderate levels have shown to

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positively modulate the expression of PSY, with a concordant increase in the carotenoids pool

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of the leaves, fruits, and roots of various plants.4 In recent years, apocarotenoids such as SL

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have been explored, which play key rhizosphere signaling roles in establishing the beneficial

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symbiotic relationship with AM fungi.4

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Fanciullino et al.20 proposed that reactive oxygen species (ROS)/redox status (redox

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signaling) and sugars/carbon status can be considered as key integrated factors that account

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for most effects of the major environmental factors, particularly in relation to environmental

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stress responses and photosynthetic metabolism, influencing the synthesis of primary and

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secondary metabolites, including carotenoids. The increased ROS production stimulates the

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enhanced biosynthesis of carotenoid through redox signaling.21 The altered biosynthesis of

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carotenoids with varied glucose levels has shown the complex mechanism of regulation in

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leaves and fruits. Poiroux-Gonord et al.22 observed that limiting the carbon supply (soluble

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sugars or total carbohydrates) to the fruit can result in substantial improvement in its

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nutritional quality, including the carotenoids of clementine (Citrus clementina) fruits.

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Fanciullino et al.20 indicated that the accumulation of high amounts of soluble sugars during 8


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the early stages of fruit development exerts a negative influence on plastid development, and

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consequently on carotenoid accumulation. However, at later stages, higher sugar

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accumulation increases carotenoid production by promoting fruit ripening, and more unlikely,

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by providing higher levels of eicosanoid precursors for carotenoid biosynthesis.

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Carotenoids in photosynthetic apparatus

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Carotenoids and Chl are functional subunits of the photosynthetic apparatus. They play a

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crucial role in photosynthetic light harvesting and photoprotection. Carotenoids are diverse,

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nearly 750 of which have been identified in photosynthetic organisms.15 However, the

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composition of major pigments is remarkably constant among the plastids of vascular plants,

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mosses, and green algae (subkingdom Viridiplantae). With a few remarkable exceptions,

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plastids of all organisms belonging to the subkingdom viridiplantae (syn. Plantae) contain

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two Chl (Chla and Chlb) and six major carotenoids, Neo, Vio, antheraxanthin (Ant), Lut, Zea,

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and β-Car.23 One of the known exceptions is Cuscuta reflexa, a parasitic plant that lacks Neo,

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and is replaced by (Z)-Vio.15 The Vio, Ant, and Zea carotenoids are involved in dynamic

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interconversion through the operation of the xanthophyll cycle, also referred to as the

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violaxanthin (VAZ) cycle (Fig. 1). Apart from these major carotenoids, other non-ubiquitous

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carotenoids have also been found as follows: i) Lut epoxide (Lx) which, together with VAZ

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pigments, also participates in a lightdriven dynamic Lx cycle in some plant species (Esteban

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& Garcia-Plazaola, 2014); ii) xanthophyll esters (-OH of xanthophylls bound with fatty

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acids); iii) α-Car, which partly replaces β-Car in some species under low light; iv)

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lactucaxanthin, which substitutes Lut in LHCs in a few plants, such as lettuce; and v) some

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red

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rhodoxanthin)

retro-carotenoids

(that

include

anhydroescholtzxanthin,

15

escholtzxanthin,

and

. Each of these pigments plays a specific role, and is distinctively located 9



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within the photosystem I (PSI) and photosystem II (PSII) of the photosynthetic apparatus.

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Figure 3 shows the pigments that occupy different locations within the protein complexes of

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each photosynthetic unit, and that play an important role in light harvesting, thermal energy

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dissipation (dissipation of excess light energy by non-photochemical quenching; NPQ), and

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photoprotective photoprotection by quenching of ROS and Chl triplets.23

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The photosynthetic apparatus dynamically adjusts to a changing environment by

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changing the structure, composition, and size of the PSII antenna, and by adjusting the PSII :

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PSI ratio. Using a meta-analytical approach, Esteban et al.23 studied how environmental/stress

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factors, including low temperature, high temperature, drought, salinity, chilling, ozone,

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carbon dioxide, and season, modulate the photosynthetic pigment composition in plants, by

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combining data from 525 papers that include 809 species (plotted in Fig. 4). Under all stress

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conditions, the ratios of Chla : Chlb, Neo : Chl, and β-Car : Chl were found to have the

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highest stability, irrespective of the stress conditions. On the other hand, total Chl (Chla +

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Chlb; per leaf area basis), xanthophyll cycle pigments (VAZ: Chl), and Lut: Chl showed more

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responsiveness to low temperature, drought, and chilling stress (Fig. 4). Notably, the total Chl

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(per leaf area basis) was the most responsive, increasing significantly under salinity and

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seasonality, whereas chilling, ozone, and drought stresses were found to reduce this pool. The

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ratios Lut : Chl, β-Car : Chl, VAZ : Chl (highest positive linear relationship), and Chla : Chlb

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correlated positively with the daily photon irradiance (DPI), whereas the total Chl per leaf

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area correlated negatively. Most remarkably, VAZ : Chl did not show a negative correlation

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with any of the stress factors studied, with the highest positive ratio under low temperature,

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followed by drought and chilling (Fig. 4). The higher responsiveness of the VAZ pigments

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under stress conditions suggested their crucial contribution to plant survival under adverse

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climatic conditions. A group of researchers previously analyzed the carotenoids and α10


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tocopherol in the photosynthetic tissues of several species, including phytoplankton, and

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observed that VAZ pigments and α-tocopherol were taxonomically ubiquitous.24 During

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evolution, the total amount of VAZ pigment decreased progressively from green algae to

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angiosperms.24 Surprisingly, the contents of α-tocopherols increased gradually during

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evolution, playing a complementary role. It is believed that in species with longer life spans

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and growth rates, the presence of membrane stabilizers such as tocopherol has provided

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additional photoprotective abilities.24

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Interestingly, irrespective of the phylogenetic trends and environmental stress

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conditions, the Neo : Chl ratio is nearly stable.23 Thus, it was suggested that this feature could

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possibly be used as reference for the improved accuracy of the quantitative analysis of

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carotenoids and chl.

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Carotenoid rich crops

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In addition to photosynthetic leaves, which were discussed earlier (Carotenoids in

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photosynthetic apparatus), chromoplasts of roots (e.g., carrots), tubers (e.g., orange flesh

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potatoes and sweet potato), flowers (e.g., marigolds), fruit (e.g., tomato), and seeds (e.g.,

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wheat, rice, barley, maize, canola, pumpkin, and sunflower) accumulate carotenoids densely

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as storage metabolites, which represent more diversity in terms of contents and

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composition.25 Chromoplasts are carotenoid-accumulating plastids in which various

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lipoprotein-containing microstructures, such as globules, crystals, membranes, fibrils, and

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tubules, sequester carotenoids.4 The microstructures provide higher light stability to the

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carotenoids.25 Moreover, the size and density of plastids in unripe fruits are directly linked to

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the carotenoid accumulation in ripened fruits.4

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According to the United States Department of Agriculture (USDA) nutrient 11



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database,26 dehydrated peppers (sweet, red, freeze-dried) are a highly abundant source of β-

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Car (428.9 µg/g), followed by dehydrated carrot (339.5 µg/g), and paprika spice (261.6 µg/g).

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Dehydrated carrot is also the most abundant source of α-Car (142.5 µg/g). Red sweet peppers

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are also rich in α-Car and β-Cry (62.5 µg/g). Raw persimmon (14.4 µg/g), winter squash,

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papaya, tangerine, and other citrus fruits are also rich in β-Cry. Paprika spice (189.4 µg/g) and

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green leafy vegetables, especially kale, spinach, sweet potato, and dandelion greens, are rich

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in Lut + Zea. Tomato is the most abundant source of LYC (459.0 mg/g DW), followed by

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rose hips (68.0 µg/g; wild from the Indian Northern Plains), guava (52.0 µg/g; raw), and

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watermelon (45.3 µg/100g; raw). In addition to those in the USDA database, the seed arils of

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Gac fruit (Momordica cochinchinensi Spreng.), the seed arils of bitter melon (Momordica

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charantia L.) fruit, and deep red fruit of Tinospora cordifolia (willd.) are established as a rich

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source of LYC, containing (200–500) µg/g FW.27–29 Moreover, apart from the carotenoid-rich

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food crops described above, the fruits of acerola, apple, grape, mango, peach, papaya,

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pineapple, grapefruit, banana, maize, orange-fleshed sweet potato, green beans, lettuce,

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mustard greens, turnip greens, collard greens, and drumstick leaves are a few other notable

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examples of carotenoid-rich food, contributing significantly to the human diet in different

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parts of the world.

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The ripe fruit of the different varieties of peppers (Capsicum sp.) (family Solanaceae),

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especially red pepper, is consumed worldwide in the form of paste, paprika, and oleoresin,

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which contain several nutritionally important carotenoids at very high concentration.30,31

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Interestingly, the accumulation of different carotenoids gives ripened fruit its distinct color.

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For example, red-fruited pepper massively accumulates six major carotenoid pigments: Ant,

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Zea, capsanthin, capsorubin, β-Cry, and β-Car. Primarily, the capsanthin and capsorubin,

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formed from Ant and Vio, respectively, are the characteristic pigments of red colored peppers, 12


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whereas the yellow fruits accumulate a significant amount of Vio. In contrast, an orange color

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is derived typically by producing high amounts of β-Car, or by producing a mixture of

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yellow- and red-colored carotenoids of Ant, capsanthin, and β-Cry (similar to red color fruits,

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but to a lesser extent).30 A similar process occurs in carrots, where the orange genotypes

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accumulate mostly α- and β-Car, the yellow genotypes store Lut, the red genotypes contain

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moderate levels of LYC, and the white-rooted genotypes contain almost no carotenoid.32 In

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recent years, rose hip fruits have been explored as a rich source of rare carotenoids

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rubixanthin, which is used as a natural food coloring compound (E161d).33 However, their

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health benefits require further investigation.

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Interestingly, with the significant difference in the composition and content of

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carotenoids in fruits, it has been shown that the morphology of chromoplasts and the physical

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deposition form of carotenoids are crucial factors in the bioavailability and bioaccessibility of

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carotenoids.34 Generally, the deposition of β-Car and LYC in the form of very small

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crystalloids in the chromoplast of papaya fruits was found to be associated with their

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significantly higher bioavailability, compared to the large crystalloids found in tomato and

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carrot. Thus, even with the low contents of LYC in papaya, compared to the tomatoes, their

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consumption can be more beneficial.

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Pre- and post-harvest cultivation factors affecting carotenoid

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content

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The metabolite composition of crop plants during the growth period (pre-harvest), and also

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during post-harvest handling, are significantly altered with changing cultivation practices and

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environmental conditions, induced by several biotic and abiotic factors.35 The nature and

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impact of metabolite changes, especially on carotenoids resulting from pre- and post13



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harvesting related factors, have been extensively studied in recent years. The reported results

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vary substantially, according to i) the genetic structure of cultivar and species; ii) pH (soil

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salinity) and available nutrients in the soil; iii) cultural and agronomic practices of the crop

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such as fertilizer application and grafting; iv) weather and climatic conditions, including

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temperature, water and light intensity, growing locations, and seasons; and v) stage of

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maturity at harvesting. Similarly, the key post-harvesting factors affecting carotenoid contents

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are the storage conditions and the postharvest processing methods.36

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Cultivar and species

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The genetic architecture of plant populations is a key controlling factor responsible for the

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variation in carotenoid composition and contents.37 Several quantitative trait loci (QTL) have

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been identified as being responsible for carotenoid variation among wheat,38,39

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(Cucumis melo L.),40 maize,37 and many others plant populations. Kandianis et al.37

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demonstrated that genetic control of maize grain carotenoid composition is coordinated

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through several QTL distributed throughout MEP, isoprenoid, and carotenoid metabolic

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pathways, most of which display pleiotropic effects. A point mutation (substitution of a

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conserved amino acid) in CLY-ε was identified in high lutein accumulating wheat species.38

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While, reduction in wild-type mRNA of PSY (by a sequence duplication and activation of a

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cryptic exon) was found to be responsible for the reduction in PSY protein and thus

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carotenoid concentration in wheat endosperm.38

melon

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Buah et al.41 studied the molecular basis of high carotenoid accumulation in the

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banana fruit of cv. Asupina (Musa group) and the low carotenoid accumulation in cv.

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Cavendish. The significantly lower expression of CCD 4 (responsible for carotenoid

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catabolism) and the higher conversion of amyloplasts to chromoplasts for enhanced storage 14


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(enhanced sink strength for effective sequestration) during banana fruit ripening was found to

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be primarily responsible for the higher accumulation of carotenoids in cv. Asupina.

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Interestingly, the transcript abundance of major biosynthetic genes, including DXS, PSY1,

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PSY2a, and LCY-β, were not correlated with carotenoid levels in mature fruit of both

319

cultivars. Thus, it was suggested that a post-transcriptional regulation of carotenoid

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biosynthetic genes may be responsible for the significantly different carotenoid levels. In

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advancements of carotenoids regulatory mechanisms, ORANGE (OR) family proteins

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mediating the post-transcriptional regulation of PSY has recently been explored.42 Zhou et

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al.42 demonstrated that OR proteins function similarly to molecular chaperones, and that this

324

assists in the proper folding of PSY for its enhanced stability and activity. The PSY and OR,

325

two crucial proteins involved in carotenogenesis, stably interact with each other within

326

plastids via the N-terminal region of the OR protein. Interestingly, these interactions do not

327

affect PSY gene expression; however, they positively modulate the active PSY protein levels

328

and carotenoid accumulations.

329

Plant domestication has involved the selection of several desirable agronomic traits,

330

the selection of genotypes that lack pod-shattering mechanisms with no dormancy, and good

331

seed storability. However, as a result of domestication processes, the nutritional values of

332

some crops have been negatively affected. For example, ABA (synthesized from carotenoids)

333

is the positive regulator of seed dormancy. Furthermore, due to the selection of legume

334

cultivars with no dormancy (low in carotenoids), the contents of total carotenoids decreased

335

48% on average in cultivated legumes when compared to their wild ancestors.43 Moreover,

336

plants with high carotenoid contents have more chances of survival in a natural condition,

337

because of the higher synthesis of carotenoid derivative volatile scent and aroma constituents,

338

such as geranyl acetone and β-ionone, which attract predators and dispersal animals.43 In 15



339

another study, the genetic factor shows the highest impact ((7–11)-fold difference) on the

340

carotenoid contents in carrots.12 In addition, climate-related factors (30%–40%), low nitrogen

341

fertilization (-8% to -11%), retail storage in ambient temperature (-70%), and heat processing

342

by boiling (-20%) have also shown significant effects on the carotenoid content in carrots.

343

Among the various varieties of carrots, purple colored carrots have been recorded as

344

containing the highest amount of β-Car (≈160 µg/g FW), followed by orange (≈85 µg/g FW),

345

yellow (0.85 µg/g FW), and only trace amounts in white varieties.12

346

Singh et al.44 studied the impact of boron (B), calcium (Ca), and genetic factors on

347

carotenoids, anthocyanins, and the antioxidant capacity of carrots. The highest contents of β-

348

Car were recorded in cv. Kuroda (orange), followed by purple, red, yellow, and white

349

cultivars. Anthocyanins were recorded in cv. Purple Dragon (purple color). The supplement

350

of B and/or Ca in the feeding solutions during plant growth influenced the accumulation of

351

other minerals such as P, K, Mg, S, and Na in carrot roots (p < 0.05). When no additional B or

352

Ca (-B or -Ca treatments) was supplied, a significant increase in the concentration of P, K,

353

and Na in the roots was observed (especially with -B treatments), with (33%–50%) increase

354

in the accumulated levels of α- and β-Car. In contrast, the highest (9.4 mg/100g FW) and

355

lowest (3.9 mg/100g FW) contents of total anthocyanins were recorded in the -Ca and -B

356

treatments, respectively. On the other hand, changes in the carotenoid levels were not

357

recorded in any studied cultivar for the case when the two minerals were not supplied

358

together (-B and -Ca treatments). The significantly low accumulation of anthocyanin in both

359

the -B and -Ca treatments, and the enhanced production in -Ca treatments suggested that

360

polyphenols and carotenoids biosynthetic pathways are independent and differentially

361

regulated by Ca and B.

362

Recently, Perrin et al. 32 demonstrated that carotenoids are differentially accumulated 16


Page 16 of 53

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363

in phloem and xylem of carrot root depending on the genotypes, with the partial association

364

between carotenoids contents and the transcriptional level of their biosynthesis-related genes.

365

Interestingly, the contents of carotenoids were higher, lower, and equal in xylem tissue,

366

compared to the phloem in the orange, red, and purple genotypes, respectively. Under

367

restricted water conditions, the amount of total carotenoids decreased in the xylem of the

368

orange genotypes, while it increased in the xylem and phloem of the purple genotypes and in

369

the phloem of red genotypes. Under these restricted water conditions, the expression pattern

370

of the carotenoid biosynthesis gene expression was not correlated with the contents of

371

carotenoids. The partial association of the gene expression pattern with carotenoids contents

372

under normal conditions, with no association under water-restricted conditions, suggested

373

that the mechanisms determining carotenoid sequestration in carrot root in the standard

374

condition are simpler than the influence of complex environmental signals, which could

375

involve the linkage of other synergic/antagonist pathways. A similar reduction in the contents

376

of carotenoids was observed in carrot roots and leaves, under combined biotic (Alternaria

377

dauci infection) and abiotic stress (restricted water conditions).45

378

Genetic factors have also shown to have a substantial influence on the carotenoids

379

content of green leafy vegetables. In a study by Baslam et al.,46 among three types of lettuce

380

consumed as salads, Lactuca sativa L. var. longifolia (commonly named Cogollos) showed

381

the highest contents of carotenoids, compared to two other cultivars belonging to the capitata

382

variety (commonly named Batavia and Maravilla). Interestingly, higher levels of carotenoids

383

were recorded in the outer (2.0 mg/g DW), than in the inner leaves ((1.1 to 1.3) mg/g DW), of

384

all three lettuce studied. The consequence of low light exposition of the inner leaves inside a

385

dense head is significantly responsible for its low contents of carotenoids and Chl. In our

386

recent study, we explored the genetic potential of the baby leaves of 23 distinct lettuce 17



387

cultivars for their health-beneficial metabolites, including major carotenoids.47 The results

388

showed that the composition and contents of the carotenoids in the lettuces varied

389

significantly between cultivars, and were principally dependent on leaf color, with the highest

390

contents in red lettuces, followed by green/red and green lettuces. Similarly, our previous

391

investigation on minimally processed ready-to-eat baby-leaf vegetables showed significantly

392

higher contents of carotenoids in red Romaine than in green Romaine.48 Significant

393

quantitative variations in carotenoid contents have also been observed in the foliage of

394

commercially grown cultivars of the drumstick (Moringa oleifera Lam) tree.49 Among the

395

various Indian cultivars studied, the highest content of total carotenoids (80 mg/100g FW)

396

was recorded in the Bhagya (KDM-1) cultivar.

397

Giuffrida et al.31 characterized the carotenoid contents of 12 different varieties of

398

Capsicum cultivars (cultivated in Northern Italy) belonging to three species (Capsicum

399

chinense, C. annuum, and C. frutescens) of various color, shape, and dimension. Among the

400

cultivars with red color, a high amount of β-Car was recorded from the fruits of Habanero,

401

Naga morich, and Sinpezon, whereas no β-Car was detected in Serrano, Tabasco, and

402

Jalapeno. Yellow colored Habanero golden and Scotch Bonnet showed a high content of Lut,

403

α-Car, and β-Car. In contrast, Habanero orange was rich in Ant (9.69%) and Zea (10.8%).

404

Giuffrida et al. proposed that the diverse metabolic pathways occurring in the different

405

cultivars were probably responsible for the altered contents of carotenoids.

406

The genetic differences between non-anthocyanin-accumulating (cv. Ailsa Craig) and

407

three anthocyanin-accumulating tomato genotypes (cv. Atroviolaceum, Atv; anthocyanin fruit

408

type, Aft; and Sun Black, SB) accounted for the substantial differences in fruit content

409

between the carotenoids and anthocyanin.50 The carotenoid contents of Atv tomatoes were

410

(2–2.5)-fold higher, relative to the other two anthocyanin-accumulating and non-anthocyanin18


Page 18 of 53

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411

accumulating genotypes. Salinity stress (5.5 dS/m) led to the further (2–3)-fold increase in

412

the LYC content in most studied genotypes. In contrast, saline treatment significantly

413

increased (2-fold) the accumulation of total anthocyanins in the fruits of high anthocyanin

414

accumulating SB (298.57 and 479.32 µg/g DW in control and treated fruits, respectively),

415

while it reduced anthocyanin (≈10-fold) in fruits of low anthocyanin accumulating Aft (54.77

416

and 60.1 µg/g DW in control and treated fruits, respectively). These observations also suggest

417

that carotenoid and anthocyanin biosynthetic pathways are independent, and differentially

418

regulated by salt stress. Also, the level of anthocyanin did not affect carotenoid contents in

419

tomato fruits. 50

420

The relative activities of LCY-β and LCY-ε are the key regulatory enzymes directing

421

the carotenoid pathway towards β-Car and α-Car, respectively. Thus, the transgenic

422

manipulations of LCY-ε expression in Arabidopsis, potato, and Brassica have been shown to

423

increase the pool of β-Car and β-xanthophylls, such as β-Cry and Zea. Naturally, maize

424

exhibits considerable natural variation for kernel carotenoids, mainly regulated by CLY-ε,

425

with some lines having yellow to orange kernels that accumulate as much as 66 µg/g of

426

carotenoids (dominated by Lut), followed by Zea, β-Car, β-Cry, and α-Car.51

427

Sufficient evidence has been reported to conclude that the genetic makeup of cultivar

428

and species is the key contributing factor that significantly affects the carotenoids in food

429

crops. Thus, in the future, the untapped pools of conventional cultivars can be characterized

430

for the contents of nutritionally important phytoconstituents, including carotenoids. The

431

knowledge of carotenoid contents and composition in different edible parts of crop cultivars

432

will be potentially useful to nutritionists, for the selection of nutrient-rich plants in food

433

formulation and for proper diet recommendation.

19



434

Soil factors: pH and available nutrients

435

The soil salinity and concentration of available nutrients may alter cellular and whole plant-

436

level physiological and biochemical processes, thus strongly influencing the contents of

437

carotenoids, and the overall antioxidant properties of fruit and vegetables.36 The nature and

438

effect of soil salinity are similar to those of drought stress, since salinity modulates the

439

imbalance of the osmotic potential in the soil-plant system to prevent the efficient uptake of

440

water. The consequences of salinity stress on carotenoids are extremely multifaceted, and are

441

attributed directly to the photosynthesis process by the stomatal closure and mesophyll

442

limitations for the diffusion of gases. Shah et al.36 evaluated the response of the leaf pigments

443

of wheat (Triticum aestivum L.) under varying levels of soil salinity and applied fertilizer, and

444

found that higher doses of fertilizer increased the contents of carotenoids and Chl across all

445

levels of soil salinity (zero to 14 dS/m). Likewise, at all levels of applied fertilizers,

446

increasing the level of soil salinity from zero to 14 dS/m concordantly increased the Chl and

447

carotenoid contents per leaf area. However, due to the plant adaptation process and defense

448

response under salinity stress, the leaves were found to be thicker and narrower. Thus, on a

449

per-plant basis, increasing salinity significantly reduced the Chl and carotenoids produced

450

across all levels of soil salinity (zero to 14 dS/m) and fertilizer treatment. Remarkably, these

451

results are not consistent with the reports by Borghesi et al.,50 who studied the effects of

452

salinity stress (5.5 dS/m) on the carotenoids and anthocyanins of tomato fruits (discussed

453

earlier in “cultivar and species” section) and recorded a (2-3)-fold increase in carotenoid

454

contents of tomato fruits on a dry weight basis. These observations suggest that the outcome

455

of stresses may vary considerably according to the plant species and plant parts

456

(vegetative/reproductive).

20


Page 20 of 53

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457

It has been reported that the pre-harvest or post-harvest application of various plant

458

growth regulators, elicitors, and fertilizers (such as K, N, Mg) beneficially regulate

459

carotenoids biosynthesis in crop plants, including lettuce, wheat, and moong (Vigna radiata)

460

seedlings, as well as muskmelon fruit.5 The foliar application of biotic elicitors, chitosan,

461

carboxymethyl chitosan, and the signaling molecules of methyl jasmonate (MeJ) and salicylic

462

acid (SA), are found to be beneficial for the substantial enhancement of major carotenoids in

463

the foliage of the field grown trees of M. oleifera.52 In this report, among the major genes of

464

the carotenoid biosynthetic pathway, the expression of LCY-β was maximumly influenced

465

after treatment with elicitors and signaling molecules, suggesting LCY-β-mediated

466

enhancement in the production of β-Car in elicitor-treated leaves. Similarly, carotenoids in

467

the foliage of coriander crop were found to increase by 6.8-fold and 5.4-fold, when treated

468

with MeJ (10 mmol/L) and SA (500 mmol/L), respectively.53

469

The germination and application of sulfur fertilization have shown a positive

470

influence of the accumulation of chlorophylls and carotenoids in radish sprouts,54 probably

471

due to the increased activity of S-adenosylmethionine (SAM), a sulfur-containing metabolite

472

required in a vital step of chlorophyll biosynthesis. The process of germination led to a 14-

473

fold increase in the Chl content in control sprouts from the second to the fifth day. After 7

474

days of cultivation, the Chl contents in sprouts treated with sulfur at concentrations of 100

475

mg/L were 88.5% higher than those in the control sprouts. Similarly, during the sprouting

476

process, the content of total carotenoids showed a remarkable increase up to the fifth day

477

after cultivation, which was 4.4 times higher than that in 1-day-old seedlings. The contents of

478

total carotenoid in sprouts under sulfur treatment also showed similar trends to that of the

479

Chl.

21



480

It is well known that the optimum supply of nutrient to crops is beneficial for

481

producing higher biomass and economic yield. In many crops, improvement in the nutritional

482

profile has been obtained following nutrient management. In the future, more rigorous

483

integrated approaches, with the combined judicious use of macro- and micro-nutrients

484

containing organic and inorganic fertilizers as well as plant growth promoters, can be

485

considered for their potential for the nutritional enhancement of crops.

486

487

Cultural and agronomic practices: grafting and organic farming

488

Grafting fruit and vegetable crops onto resistant rootstocks is an effective tool for

489

manipulating the susceptible scion morphology in order to control soil-borne diseases and

490

other environmental stresses. Interestingly, improvements in visual appearance, texture, and

491

nutritionally important metabolites have also been reported as a result of the translocation or

492

modification of the physiological processes of the scion. Grafting has been shown to improve

493

LYC and β-Car contents by 20%–40% in tomato and watermelon fruit,55 driven by high

494

potassium (K) concentration, which is involved in protein synthesis and the enhanced activity

495

of acetic thiokinase (Ligases). This enzyme is involved in the formation of acetoacetyl CoA,

496

a molecule involved in the biosynthesis of isopentenyl diphosphate (IPP), a precursor of

497

carotenoids from the mevalonic acid pathway.55 Also, K may be involved in the enhanced

498

biosynthesis of carotenoids by up-regulating carbohydrate metabolic enzymes such as

499

pyruvate kinase and phosphofructokinase.55

500

Condurso et al.56 tested several Cucurbita maxima×Cucurbita moschata hybrids and

501

two genotypes of melon (Cucumis melo L.) for their disease resistance and nutritional

502

improvement of melon fruit (cv. Proteo). The use of pumpkin hybrid rootstocks showed a

503

significant improvement in the qualitative and quantitative carotenoid profiles with the 22


Page 22 of 53

Page 23 of 53


504

presence of Lut ((5.5–13.7) µg/g FW) in fruit samples, with a higher amount of β-Car (≈8-

505

fold higher than control) and α-Car (≈56 % higher than control). Meanwhile, the melon

506

genotype rootstocks showed a significant decrease in β-Car (≈55% less than the control).

507

Interestingly, the absence of Lut and β-Car (major carotenoids of pumpkin) in non-grafted

508

melon fruits and their significant presence in melon fruits obtained from pumpkin as

509

rootstocks, indicated that metabolites associated with fruit nutritional quality are translocated

510

to the scion through the xylem.

511

Cardoso et al.57 compared the contents of carotenoids between three fruits

512

(Persimmon, acerola, and strawberry) produced by organic and conventional farming. In

513

acerola, the conventional production showed significantly higher contents of β-Car (61.3

514

µg/g) compared to organic fruit (24.8 µg/g). Meanwhile, no significant difference in the

515

carotenoid content was observed for persimmon and strawberry fruit produced by different

516

farming systems. The higher contents of β-Car in acerola fruit produced by conventional

517

production probably resulted from soil fertilization, which is known to affect the biosynthesis

518

of carotenoids. Pertuzatti et al.58 also recorded a significantly high amount of carotenoids in

519

conventionally grown yellow passionfruit (Passiflora edulis) (25.10 mg/100 g) as well as

520

organic passionfruit (13.99 mg/100g).

521

Cultural practices, especially grafting, have shown promising results for the

522

qualitative and quantitative improvement of carotenoids in crop plants. However, only limited

523

research has been carried out on these aspects. Thus, in the future, suitable rootstocks and

524

rootstock/scion combinations capable of having a positive impact on nutritional and

525

agronomic parameters can be identified. Moreover, the mechanism of nutrient translocation

526

to the scion should be explored.

527

23



528

Weather and climatic factors: temperature, water intensity, light intensity,

529

growing locations, and seasons

530

Weather and climatic factors, including low temperature, high temperature, drought, chilling,

531

ozone, carbon dioxide, and season significantly modulate the photosynthetic pigment

532

composition in plants, as shown in Fig. 4. Similar to photosynthetic leaves, these factors have

533

been shown to significantly modulate the fruit, roots, and tuber carotenoids. Lu et al.59

534

observed significant variance in carotenoid contents (yet similar profiles) among the red-flesh

535

navel orange “Cara Cara” fruit from the different growing regions of Hubei, Fujian,

536

Chongqing, Jiangxi, and Hunan in China, the variances of which are mostly attributed to the

537

environmental conditions. The ambient temperature was found to be positively correlated (p

538

= 0.697; only if average temperature does not exceed 21 °C), with the total carotenoids

539

content of “Cara Cara”. Specifically, the highest total carotenoid content of 1,295.48 µg/g

540

(DW) was found in Fujian “Cara Cara”, with the lowest content detected in the samples from

541

Hunan (989.49 µg/g DW). Surprisingly, no correlation was found between the total

542

carotenoid content and the lighting time of different locations, indicating the complicated

543

relationship between environmental conditions and carotenoid content.

544

Payyavula et al.13 measured the phenylpropanoids and carotenoids, along with the

545

expression of several structural genes, in purple potatoes grown in environmentally diverse

546

locations of Alaska (latitude and longitude of 51.3–71.8° N and 130° W–172° E), Texas

547

(33.3° N and 101.5° W), and Florida (29.4° N and 81.3° W). Phenylpropanoids, including

548

chlorogenic acid, and anthocyanin were higher in samples from the northern latitudes, with a

549

concordant expression of phenylalanine ammonia lyase, chalcone synthase, and sucrose

550

synthase. The long photoperiods with unique UV-B and red to far-red light ratios, as well as

551

the cooler nights of the northern latitudes might have positively influenced the 24


Page 24 of 53

Page 25 of 53


552

phenylpropanoid biosynthesis compared with the same plant species in the south. In contrast,

553

only a minor variation was observed for total carotenoids; however, the carotenoids

554

composition showed a significant difference among the growing locations. For example, Vio

555

was the major carotenoid in all Alaskan samples (1.2–1.8 µg/g), contributing more than 50%

556

of the total carotenoids. However, Florida tubers contained only 0.1 µg/g Vio (3.5%) which,

557

in contrast to the Alaskan samples, had higher amounts of Zea, probably due to the de-

558

epoxidation of Vio to Zea (VAZ cycle). Interestingly, neither ZEP nor VDE was differentially

559

expressed in the Florida potatoes compared with the other samples, suggesting the differences

560

were not due to the transcriptional regulations of these two genes. The experimental results

561

suggest that the higher contents of ascorbate in the Florida samples were responsible for the

562

de-epoxidation of Vio to Zea. Similarly, Lut dominated in the Texas tubers (50% of total

563

carotenoids), with a concordant higher expression of LCY-ε, which catalyzes the ε-

564

cyclization of LYC and modulates the carotenoid biosynthesis towards α-Car branch.

565

Zhong et al.35 investigated the impact of environmental variations on carotenoid

566

accumulation in the carrot leaves and roots grown during two different periods of favorable

567

(mean temperature of 18.4 °C and a global ray of 1.8 J cm−2) and less favorable (14.6 °C and

568

1.3 J cm-2) cultivation conditions. In taproots and leaves, carotenoid contents were 20%–50%

569

lower in the less favorable growing conditions, with relative contents conserved on all the

570

genotypes, suggesting a common regulatory mechanism of carotenoid biosynthesis. The

571

down-regulation of all the major carotenoid biosynthetic genes under environmental

572

constraints demonstrates that carotenoid accumulation was regulated at the transcriptional

573

level. Interestingly, in roots, the decrease in α-Car and Lut contents was accompanied by an

574

increase in β-Car contents. Concordantly, at the transcriptional level, LCY-β and ZEP

575

expression increased, whereas LCY-ε expression decreased in the less favorable conditions, 25



576

suggesting the switching of carotenoid biosynthesis toward the β-branch, which probably

577

improves plant survival at low-temperature conditions.

578

It has been widely shown that high light can significantly enhance the Zea contents in

579

plants, through the VAZ cycle. However, it is interesting to note that the presence of other

580

metabolites (e.g., ascorbate) is necessary for conversion. Physiologically, VDE is a soluble

581

and inactive enzyme at neutral pH, and is activated by the acidification of the thylakoid

582

lumen, where it binds to its violaxanthin substrate and to ascorbate as a co-substrate.60 Thus,

583

with the presence of higher ascorbate, higher levels of zeaxanthin can be obtained,

584

irrespective of the transcript changes of VDE. In many reports, results have shown significant

585

alteration in the carotenoids composition, irrespective of transcriptome changes, which is

586

probably the due to the similar phenomenon of enzyme activation and inactivation at

587

particular physiological conditions. Also, the post-transcriptional regulations may be

588

responsible for the activation and stability of the carotenoid biosynthetic genes responsible

589

for the enhanced biosynthesis of carotenoids without affecting the transcripts levels.

590

591

Stage of maturity at harvesting

592

The stage of maturity of a crop harvest is the most significant factor affecting the carotenoid

593

contents and compositions, with the ripened tomato being a notable example. As discussed

594

earlier (in “carotenoid biosynthesis and its regulation by environmental factors” section),

595

mature unripe (green) fruits contain leaf-like xanthophylls (mainly Lut, Neo, and β-Car),

596

which during ripening transform into carotenes (mainly LYC and β-Car).11 In addition to the

597

carotenoids, other nutritionally important phytoconstituents (such as α-tocopherol) as well as

598

the ratio of polyunsaturated fatty acids to saturated fatty acids (PUFAs : SFAs) increase

599

significantly during the ripening of tomato fruit.61 Coyago-Cruz et al.62 observed the 26


Page 26 of 53

Page 27 of 53


600

significant effect of cluster position, developmental stage, and season (autumn and spring) on

601

the carotenoids contents of cherry tomato (cv. Lazarino and Summerbrix), while carotenoids

602

did not change significantly with irrigation and variety. In most cases, 50%–70% higher

603

carotenoids contents were found in the larger cluster. The lower levels of carotenoids were

604

observed in the autumn season, probably because of a decrease in photosynthesis under low

605

temperatures, and the short photoperiod during the autumn season.

606

Atkinson et al.63 studied the combined effect of water stress and infection with plant-

607

parasitic nematodes on the nutritional contents of tomato harvested from different positions

608

(truss 2 and 5). Truss 2 was a lower region of the plant that produced fruit at an early stage

609

(ripening approximately 108 days after sowing). Truss 5 was at the top of the plant, and the

610

fruit developed later (ripening approximately 126 days after sowing). The untreated (control)

611

tomato fruit harvested from truss 2 showed a significantly higher amount of LYC (11.29

612

mg/100g FW) and β-Car (0.87 mg/100g FW), compared to fruit harvested from truss 5 (7.58

613

mg/100g FW and 0.57 mg/100g FW, respectively). During the ripening of the truss 5 fruit,

614

nematode stress was more severe, since their juvenile offspring reinfected the plant root. The

615

LYC concentration was significantly lower (30%–35%) in truss 2 fruits that were exposed to

616

water deficit or joint stress (with nematode infection). Meanwhile, the carotenoid

617

concentration was not affected by nematode stress alone. Interestingly, in the truss 5 fruit,

618

water stress reduced the LYC contents similarly to that in the truss 2 fruit; however, the joint

619

water and nematode stress had no effect. This shows that the occurrence of biotic stress can

620

potentially interfere with the normal abiotic stress responses. The higher production of ABA

621

in response to water stress in the tomato plant was probably responsible for the reduced

622

carotenoid levels.

623

Leafy vegetables harvested at young stages, called baby leaf vegetables (BLVs), 27



624

have shown higher nutrient content, including carotenoids, compared with more commonly

625

used vegetables.64 Pinto et al.65 monitored the changes in carotenoids at 5 stages of lettuce

626

growth, grown in three different greenhouse experimental fields. In general, the contents of

627

chlorophylls and carotenoids decreased during lettuce growth; consequently, high nutritional

628

value was observed at younger stages. Interestingly, the magnesium (Mg) level decreased in

629

all the lettuces during the study period, which might have influenced the decrease of

630

chlorophyll content by a reduction in the photosynthesis rate. On the other hand, in kale

631

(Brassica oleracea L. var. acephala), mature fully expanded leaves have been shown to

632

accumulate higher contents of carotenoid than immature or “baby” leaves, with senescent

633

leaves having the lowest amount of carotenoid, probably because of the degradation of light

634

harvesting complex II at a faster rate during senescence.66

635

636

Postharvest Storage

637

The seed membrane and oil extracted from ripened Gac (Momordica cochinchinesis, Spreng)

638

fruit are considered excellent sources of bio-accessible carotenoids, especially LYC and β-

639

Car. Considerable variation has been recorded for the carotenoids contents in Gac aril in the

640

range of about 0.380–3.053 mg/g for LYC and 0.080–0.836 mg/g for β-Car.27 The influence

641

of Gac fruit and Gac oil storage on the stability of carotenoids was studied, as well as the

642

degradation kinetics under different storage conditions of 5, 45, and 60 °C,27 and it was

643

suggested that Gac oil can be better preserved using antioxidant (0.02% v/v of butylated

644

hydroxytoluene) followed by inert atmosphere (with a stream of nitrogen). However, Gac oil

645

is not as well preserved at low-temperature condition (e.g., 5 °C), which could result in a

646

reduction of the carotenoid content of the Gac oil. LYC and β-Car in the control Gac oil

647

degraded following the first-order kinetic model. Interestingly, LYC degraded faster than β28


Page 28 of 53

Page 29 of 53


648

Car, probably because of its higher singlet oxygen quenching ability than that of β-Car. It has

649

been reported that the matrix has a significant influence on the deterioration of carotenoids,

650

wherein the presence of a minimum amount of oxygen in the liquid system, compared to

651

solid and aqueous phases, was responsible for the low degradation of the carotenoids in oil

652

system.27

653

Fresh horticultural crops, including many fruits and vegetables, are treated with low

654

effective doses of UV-C light irradiation (UV-C hormesis) to activate the mechanisms against

655

senescence as a way to extend their shelf life. UV-C hormesis helps in controlling the growth

656

of spoilage organisms, while it also slows down the senescence process in plant foods, thus

657

delaying the ripening of fresh fruits and vegetables while improving the nutritional

658

contents.67 The LYC and (Z)-LYC contents in the breaker tomato increased significantly

659

following UV-C hormesis (3 kJ/m2 for 3 h), while the β-Car levels decreased.67 However,

660

when UV-C was applied for 12 h (12.2 kJ/m2), the highest significant percentage of (Z)-LYC

661

(18.5%) was observed, and the (all-E)-LYC contents showed no significant difference, which

662

could be associated with UV-C-induced photoisomerization, since light exposure leads to the

663

isomerization of (all-E)-isomers. These results indicated that UV-C light might be a specific

664

regulator of LYC synthesis under specific conditions.

665

666

Postharvest processing

667

Owing to their highly unsaturated structures, carotenoids are extremely prone to oxidation,

668

isomerization, and degradation, especially in processed food. In food, carotenoids are

669

degraded by several mechanisms, including pathways induced by heat, light, singlet oxygen,

670

acids (pH), and metals (iodine and iron).68 Thermal treatment of carotenoids in a reactive

671

environment (e.g., the presence of oxygen) results in the formation of various mono-(Z)29



672

isomers, di-(Z)-isomers, volatile compounds, and larger non-volatile compounds, which

673

results in a decrease or complete loss of biological activities. The fate of carotenoids during

674

thermal processing is influenced by a variety of factors, such as the technique and

675

methodology used, the exact experimental conditions of temperature and duration, the nature

676

of the food matrix, and by the chemical structures. Among the structural parameters, the

677

presence of –OH groups, position and numbers of unsaturated double bonds, geometric

678

configuration, and degree of esterification of carotenoids have shown to influence the

679

stability of carotenoids during thermal processing. In contrast to the carotenoids degradation,

680

methods of cooking and processing (including boiling, steaming, microwaving, frying, and

681

baking) may enhance the extractability of phytochemicals, as a result of the matrix softening

682

effect. This effect is caused by the breakdown of the cellulose structure of the plant cell as

683

well as the denaturation of carotenoid-protein complexes, which can produce a higher

684

quantitative value of the retention percentage of carotenoids from processed food compared

685

to fresh products.69,70 Thus, to a large extent, the net results of carotenoids degradation are

686

counterbalanced by the higher extraction, especially during mild cooking and processing.

687

Kotíková et al.71 investigated the impact of thermal processing on the profile,

688

quantity, and stability of carotenoid in 22 color-fleshed potato cultivars grown in the Czech

689

Republic. The yellow cultivars showed a much higher carotenoid content (26.22 µg/g DW),

690

with Ant as the main carotenoid representing 28% of the total carotenoid content, followed

691

by Neo (22%), Vio (21%), (Z)-Neo (9%), Lut (8%), β-Cry (5%), and luteoxanthin (5%).

692

Thermal processing significantly impacted all potato cultivars. Boiling (100 °C for 20 min)

693

decreased the total carotenoids content by 92% compared to baking at 180 °C for 45 min

694

(88 %). Lut was the comparatively more stable carotenoid against thermal processing

695

(decreasing by only 24%–43%), followed by β-Car (decreasing by 78%–83%), whereas the 30


Page 30 of 53

Page 31 of 53


696

other carotenoids were almost completely degraded. As expected, xanthophyll esters appear

697

to be temperature resistant, particularly in the case of baking. The higher thermal stability of

698

hydroxyl carotenoids (e.g., Lut), compared to carotenes (e.g., β-Car), has been demonstrated

699

in other systems. In a model system, zeaxanthin was found to be the most stable carotenoid,

700

followed by Lut, β-Cry, and β-carotene, with the activation energies of 65.6, 38.9, 33.9, and

701

8.6 kJ/moL, respectively.72 In general, the decreasing number of coplanar conjugated double

702

bonds and the presence of hydroxyl groups (e.g., Lut and Zea) in carotenoids decreased their

703

reactivity in radical-scavenging reactions, implying that hydroxy-carotenoids were more

704

stable than carotenes.72 Thus, β-Car is less stable than β-Cry, with a more complex

705

degradation mechanism. Similarly, in Lut and Zea, both sides of the rings are –OH-

706

substituted. However, Lut exhibits ring –OH-substitution on both sides (ε- and β-rings), and

707

thus shows more stability than Zea. Moreover, Zea has more coplanar conjugated double

708

bonds than Lut, which provides higher thermal stability.

709

Interestingly, Cueto et al.73 also observed the higher heat stability of Zea compared to

710

Lut, in an experiment that comparatively evaluated the impact of various methods and

711

formulation on individual carotenoid loss in traditionally prepared cornflakes, and those

712

prepared by extrusion. The first step in the traditional process (maize grits cooking) caused

713

60% and 40% degradation of Lut and Zea, respectively, showing that Lut is more susceptible

714

to thermal treatment. In the last step, after toasting (230 °C for 90 s), the total loss was nearly

715

80% for both carotenoids. The extruded maize in the plain formulation caused 35%

716

degradation of these carotenoids. However, in samples containing quinoa, the degradation

717

reached 60%, and formulations containing chia recorded the highest degradation of 80%.

718

These observations show that the carotenoid degradation during extrusion varied among the

719

formulations, modulated by the presence of other compounds. For example, Chia seeds 31



720

contain a high proportion of polyunsaturated fatty acids along with a comparatively low level

721

of tocopherol; thus, under thermal treatment, they can be easily oxidized, and favor the

722

production of peroxides and other free radicals that are possibly responsible for the loss of

723

antioxidant carotenoids.73

724

In fruit and flowers, most xanthophylls are found to be esterified with fatty acids that

725

promote the sequestration of xanthophylls and prevent its degradation.5 Moreover, esterified

726

carotenoids have shown increased stability, compared to the corresponding non-esterified

727

carotenoids.74 β-Cry has a highly unsaturated structure, whereby its molecule is very unstable

728

against heat. These results suggest that the esterification of –OH groups of β-Cry with fatty

729

acid might stabilize the compound against heat. Fu et al.75 observed that β-Cry esters,

730

including β-Cry laurate, β-Cry myristate, and β-Cry palmitate, are more stable than free β-

731

Cry during thermal treatment. However, the antioxidant activities of β-Cry in free or

732

esterified form did not significantly differ, probably due to their identical chromophore

733

structures. These results suggest that while the esterification of –OH groups with fatty acids

734

might not participate in the antioxidant activity of β-Cry, it stabilizes β-Cry against thermal

735

degradation.

736

The carotenoid degradation, color degradation, and furosine formation in apricot fruit

737

were observed using the first, zero, and zero order kinetic model, respectively, during the

738

convective heating at 50–70 °C.74 The major carotenoids in fresh apricot fruit were recorded

739

as (all-E)-β-Car (65%), followed by β-Cry (11%), 13-Z-β-Car (9%), 9-Z-β-Car (7%), Vio

740

(5%), Lut (2%), and Ant (about 1%). The Vio and Ant were found to be the most susceptible

741

to thermal treatment. The activation energy for carotenoids degradation ranged from 73.7

742

kJ/mol for 13-Z-β-Car to 120.7 kJ/mol for Lut.

743

It has been well documented that chemical structure and conformation determine the 32


Page 32 of 53

Page 33 of 53


744

stability of carotenoids in food systems. However, some researchers have reported different

745

outcomes, which could be linked with the physiochemical properties of food. Burt et al.76

746

observed the significant impact of dehydration techniques, genotypic factors, and storage

747

conditions on the retention of carotenoid maize kernels. The results showed that carotenoid

748

accumulation in maize is generally highest in the endosperm, whereas the embryo contributed

749

very little to the carotenoid content of the grain. Surprisingly, in a dehydration experiment,

750

carotenoid loss at 90 °C was similar to that at 25 °C, indicating that high heat drying is not

751

significantly detrimental to the carotenoids of maize kernels. During the storage of

752

dehydrated kernels at 4 °C, the carotenoid levels decrease significantly from the initial levels

753

of between 3 and 6 months of storage, but then remain stable for another year. The

754

degradation pattern (relative decline) was similar to that of major carotenoids (Lut and Zea).

755

Leong et al.77 studied the effects of processing, i.e., heating (blanching; 98 °C, 10

756

min), freezing (-20 °C), and freeze-drying on carotenoids on summer fruits and vegetables,

757

including cherry, nectarine, apricot, peach, plum, carrot, and red bell pepper. The result

758

showed that the content of carotenoids after processing was the net result of the combined

759

increase in extractability, and loss by degradation and leaching. Heating and freeze-drying

760

decreased the content of carotenoids in most vegetables studied, while the carotenoid content

761

was maintained during the freezing process.

762

In addition to the major factors influencing carotenoids degradation, water activity is

763

a crucial parameter. High concentrations of oxygen have been shown to be associated with a

764

higher rate of carotenoid degradation in dried sweet potato flakes. Bechoff et al.78 evaluated

765

the effects of storage temperature (10–40 °C), water activity (0.13–0.76), and oxygen level

766

(0–21% oxygen) during the storage of dried sweet potato chips. Over the range studied, all of

767

the factors had a marked effect on β-Car degradation. However, the effect of water activity on 33



768

β-Car breakdown was significantly less than the effect of temperature, with rate constants of

769

0.0029–0.0405 day-1. The linear relationship (R2 = 0.975) between the oxygen level and

770

degradation rate of β-Car demonstrates that oxygen could be considered as a co-substrate (if

771

present in excess) of oxidative degradation during storage. It also suggests that carotenoid

772

degradation in dried sweet potato is caused by autoxidation, due to the trend in the β-Car

773

degradation rate in relation to water activity or oxygen level. Moreover, norisoprenoids,

774

namely β-cyclocitral, β-ionone, 5,6-epoxy-β-ionone, and DHA, were identified as trans-β-Car

775

breakdown products during storage.

776

In leaves, Zea is a less-abundant carotenoid, as most of its pool is rapidly converted

777

to the carotenoid Vio via Ant, due to its involvement in the operation of the VAZ cycle.

778

Esteban et al.14 developed various pre-harvest and post-harvest stress strategies to

779

significantly enhance the contents of zeaxanthin in a spinach (Spinacia oleracea L.) and

780

rocket (Eruca sativa Mill.) based diet. In the first step, fresh weight production and VAZ

781

pigment were enhanced by high light stress (600 µmolm-2 s-1). In the second step, vinegar

782

dressing on the rocket (after illumination of 63.3 and 760.6 µmolm-2 s-1 for spinach and

783

rocket, respectively) helps to stabilize the VAZ pigments by preventing the activation of the

784

VDE enzyme.

785

A set of multiple mechanisms is responsible for the degradation of carotenoid in

786

food. It is therefore crucial that the precise mechanisms of carotenoid degradation in each

787

product are revealed, and also that ingredient formulations are ensured for carotenoid stability

788

over the shelf-life of the food.

789

In conclusion, a large number of cultivation, environmental, and genetic factors

790

influencing the carotenoid content and composition of crop plants have been explained. The

791

genetic and climate-related stress factors showed the most significant influence on the 34


Page 34 of 53

Page 35 of 53


792

composition and contents of carotenoids compared to the cultivation method factor. The

793

enhanced accumulation of carotenoids under environmental stress, such as high light, drought,

794

salinity, and chilling, is due to the complex phenomenon of a higher regeneration of

795

carotenoids, which compensates for the losses mediated by these stresses (e.g., photo-

796

oxidation and catabolism to produce ABA and SL). The potential usefulness of the stress-

797

concept for the enrichment of carotenoids in harvested food crops needs to be further

798

investigated. Also, integrated, robust, and sustainable strategies similar to those by Esteban,

799

et al. can be utilized, in which Zea and foliage biomass were enhanced by pre-harvest high

800

light stress followed by post-harvest illumination.14

801

It has been well established that high light can significantly enhance the Zea contents

802

in plants, through the VAZ cycle. The activation of the VAZ cycle enzyme VDE at acidic pH

803

in the presence of ascorbate has also been revealed. Thus, significant alteration in the

804

composition of VAZ may be possible by enhancing the ascorbate levels in crop plants,

805

irrespective of transcriptome changes. A similar phenomenon of enzyme activation and

806

inactivation may exist for other enzymes of biosynthetic carotenoids, which needs to be

807

explored. Similarly, several reports have shown the regulation of carotenoids accumulation,

808

regardless of the abundance of transcriptional levels of their biosynthesis-related genes. On

809

the other hand, some studies have demonstrated the transcriptional regulation of carotenoid

810

accumulation under biotic and abiotic stress conditions. These inconsistent observations

811

suggest the existence of several parallel pathways of carotenoid biosynthesis and catabolism.

812

Primarily, the post-transcriptional regulation (via protein–protein interaction) has recently

813

been explored for the activation and stability of PSY, a key rate-limiting enzyme responsible

814

for enhanced biosynthesis of carotenoids without affecting the transcripts levels.

815

The chemical structures, geometric configuration, and degree of esterification of 35



816

carotenoids have been shown to significantly influence the sequestration of carotenoids in

817

chromoplast, as well as thermal stability during processing. The physiological significance of

818

the occurrence of Cis (Z) forms of Neo in the photosynthetic apparatus is not elucidated at the

819

molecular level. Thus, further detailed understanding of the structure-function relationship of

820

carotenoids will assist in the exploration of the evolutionary architecture of plants.

821

822

Acknowledgment

823

This paper was supported by the KU research professor program of Konkuk University,

824

Seoul, Republic of Korea.

825

826

Conflict of interest

827

The authors have no conflict of interest to disclose.

828

829

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830

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1078

Figure captions

1079

Fig. 1. Biosynthetic pathway of carotenoids in plants, showing the linkage with 2-C-methyl-

1080

D-erythritol 4-phosphate (MEP) pathway, and other catabolic routes, to produce plant

1081

hormones and apocarotenoids. The major enzymes controlled by environmental factors are

1082

displayed. The xanthophyll (VAZ: violaxanthin + anteraxanthin + zeaxanthin) cycle is

1083

modulated by light stress, as shown in the box. NCED: 9-cis-epoxycarotenoid dioxygenase;

1084

ROS: reactive oxygen species.

1085 1086

Fig. 2. (a) In dark-grown seedlings, the higher ratio of phytochrome-interacting factor 1

1087

(PIF1): long hypocotyl 5 (HY5) represses the transcription of phytoene synthase (PSY).

1088

When the seedlings are exposed to light, a high R/FR ratio shifts the equilibrium to the active

1089

phytochrome form (Pfr), which degrades the PIF1, thus promoting the rapid derepression of

1090

PSY. (b) A candidate gene Daucus carota DCAR_032551, 1-deoxyxylulose-5-phosphate

1091

synthase (DXS), and HY5, and root de-etiolation promote the higher accumulation of

1092

carotenoids in the chromoplast of carrot taproots. However, when these roots are exposed to

1093

light, chromoplast-containing carotenoids differentiate into chloroplasts, resulting in

1094

increased ratio of chlorophylls: carotenoids.

1095

(c) During tomato fruit ripening, developmentally-controlled degradation of chlorophylls

1096

reduces the self-shading effect. Hence, a high R/FR ratio shifts the equilibrium to the active

1097

Pfr form, which degrades the PIF1, thus promoting the rapid derepression of PSY, resulting in

1098

massive accumulation of carotenoids.

1099 1100

Fig. 3. A simplified representation of the composition of chlorophylls (Chla and Chlb) and

1101

carotenoids in photosystem I (PSI) and photosystem II (PSII). CCI: Core complex I; LHCI: 47



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1102

Light harvesting complex I; CCII: Core complex II; Lhcb 4-6: Minor light-harvesting Chla/b-

1103

binding protein; (LHCII)3: Major trimeric light-harvesting complex II; β-Carotene: β-Car;

1104

Lutein: Lut; Neoxanthin: Neo; VAZ: violaxanthin + anteraxanthin + zeaxanthin. Zeaxanthin

1105

(Zea) can also be present as free in the thylakoids.

1106 15

1107

Fig. 4. Illustrations showing the major results of meta-analysis study

1108

(positive: +; negative -; and no influence: o), of low temperature (LT), high temperature (HT),

1109

drought (D), salinity (Sa), chilling (Ch), ozone (O3), carbon dioxide (CO2), and season (S) on

1110

the content of total chlorophylls (Chla + Chlb) and carotenoids of terrestrial plants. Lutein:

1111

Lut; VAZ: violaxanthin + anteraxanthin + zeaxanthin; β-Carotene: β-Car; Neoxanthin; Neo.

48


: the response

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Significance of Genetic, Environmental, and Pre- and Postharvest

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