New insights into molecular mechanism underlying seed size control

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New insights into molecular mechanism underlying seed size control under drought stress meng-jiao Lv, wen wan, fei yu, and Lai-Sheng Meng J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.9b02497 • Publication Date (Web): 12 Aug 2019 Downloaded from pubs.acs.org on August 13, 2019

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Journal of Agricultural and Food Chemistry

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New insights into molecular mechanism underlying seed size

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control under drought stress

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Running title: water-deficient stress influences seed size

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Meng-Jiao Lv1†, Wen Wan1, Fei Yu1 and Lai-Sheng Meng1*

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1. The Key Laboratory of Biotechnology for Medicinal Plant of Jiangsu Province,

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School of Life Science, Jiangsu Normal University, Xuzhou, Jiangsu, 221116,

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People’s Republic of China.

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2. Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming

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Institute of Botany, Chinese Academy of Sciences, Kunming 650201, China.

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†These authors contributed equally to this work.

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*Corresponding

authors: [email protected];[email protected]

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ORCID:

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Lai‐Sheng Meng: 0000-0002-9704-4944

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ABSTRACT

ACS Paragon Plus Environment


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In higher plants, seed size is an important parameter and agricultural trait in many

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aspects of evolutionary fitness. The loss of water deficiency-induced crop yield is the

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largest amongst all natural hazards. Under water-deficient stress, the most prevalent

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response to terminal stress is to accelerate the early arrest of floral development, and

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thereby to accelerate fruit/seed production, which consequently reduces seed size.

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This phenomenon is well known, but its molecular mechanism is not well reviewed

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and characterised. However, increasing evidences have indicated that water-deficient

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stress is always coordinated with three genetic signals (i.e. seed size regulators, initial

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seed size and fruit number) that decide the final seed size. Here, our review presents

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new insights into the mechanism underlying cross-talk water-deficient stress signaling

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with three genetic signals controlling final seed size. These new insights may aid in

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preliminary screening, identifying novel genetic factors and future design strategies,

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or breeding to increase crop yield.

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Key words: seed size, water-deficient tolerance, three kinds of genetic signals (seed

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size regulators, initial seed size and fruit number).

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Introduction

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In plants, seed size is a key factor for evolutionary fitness and a crucial agronomic

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trait in crop domestication. Crop seeds are one of the most important products for

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consumption. Thus, seed size should be one of the most significant traits that


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determine crop yield. In crop breeding, the plants of crops have been screened for

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larger seed mass/size during domestication.1,2

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Seed growth is affected through environmental and genetic signaling from

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zygotic and maternal tissues which finally determine seed size.3 Seed size regulator is

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considered as a kind of endogenous genetic signaling of plants. This kind of genetic

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signaling maternally controls seed size, which has been well reviewed in plants4-7. By

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contrast, this kind of genetic signaling also controls growth and development of

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endosperms, which have been characterised to regulate seed growth and development

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zygotically and determine final seed size in Arabidopsis8-10. Though so, the molecular

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mechanism underlying the interaction of environmental stress with this kind of

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genetic signaling to determine final seed size is not well reviewed and characterised.

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The initial seed is other kind of endogenous genetic signaling of plants. The

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larger the initial seed is, the more drought-resistant the germinating seedling will

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be3,11,13. Therefore, a positive correlation exists between seedling/plant establishment

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and initial seed size. Evolutionary biologists and ecologists observed this

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phenomenon early11. That is, the seedlings of large-seeded plants can withstand

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water-deficient stresses, whereas plants with small seeds are efficient colonisers

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because they can produce a considerable number of seeds3,11,12. Interestingly, Ref3,11,12

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revealed that the trade-off between grain size and number in rice is coordinated by the

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GRAIN SIZE AND NUMBER1–mitogen-activated protein kinase cascade by

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integrating localised cell proliferation and differentiation. Though so, relative

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molecular mechanism is not well characterised and reviewed.



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The fruit number is the third kind of endogenous genetic signaling of plants.

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Fruit number may affect on final seed size. Fruit number can considerably determine

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life span. As a well-known fact14-17, fruit production is an important factor controlling

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meristem arrest and life span in different species which determine seed filling and in

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turn influence seed size. For example, in several monocarpic plants, with the

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production of a certain fruit number, meristem activity will be arrested, which is

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coordinated with preceding completion of seed/fruit filling17, thereby influencing final

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seed size. This strategy can optimise the allocation of resources to seed production.

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However, the underlying molecular mechanism is largely unclear and need be further

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characterised.

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Taken together, water-deficient stress interplaying with three kinds of genetic

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signals (seed size regulators, initial seed size and fruit number) may control final seed

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size. This may be an evolutionary strategy adopted by plants to maximize the

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opportunities of seed production and species continuation under water-deficient

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conditions, which affects on final seed size. However, the underlying molecular

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mechanism is not fully reviewed and characterized.

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Here, we will review the increasing evidence presenting the relative

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mechanism. Genetic and/or biochemical mechanisms underlying interaction or

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cross-talk between water-deficient stress response and three genetic signals will be

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considered. Finally, the potential application of the complex interaction in agriculture

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will be discussed.


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Arabidopsis ANGUSTIFOLIA3 (AN3)–YODA (YDA) signal transduction

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pathway

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AN3 which encodes a transcription coactivator is a member of a small gene family18.

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AN3 is expressed well in the embryo and seed coat7,18. The lack of AN3 (an3) within

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a species (Arabidopsis) generates large seed size and increases the fruit number.

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Therefore, AN3 can be effectively utilized to analyse the molecular mechanism

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underlying the affect of water-deficient stress on seed size (Figure 1)5-7,13,18,19.

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Given that the seedlings of large-seeded plants can withstand water-deficient

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stresses,11 and an3 mutants present large initial seed size7, the reason why an3

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seedlings have large seed size under water-deficient tolerance has been explored.

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Large initial seed size of an3 mutants produced an3 seedlings with elongated

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roots13,18. And this kind of an3 seedlings also showed high water-use efficiency and

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water-deficient tolerance caused by sugar/light signal-mediated decrease in stomatal

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density and sugar/light signal-mediated enlarged root system by transrepressing either

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YDA or constitutive photomorphogenic 1 expression13,18. Therefore, this kind of an3

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seedlings can resist water-deficient stresses well18. Further analysis finds that during

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an3 seed maturation, osmotic stress can significantly alter sugar levels7. an3 seed

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maturation may be thus accelerated because a low hexose/sucrose ratio is significantly

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correlated with seed filling and cell elongation during late seed development

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(maturation phase)21. As a result, this kind of an3 seedlings produce large



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seed/cotyledon size relative to wild-type under osmotic stress (Figure 1)7.

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The increased fruit number in an3 mutants also suggests delayed meristem arrest

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and long life span that coordinate with large seed size (or cotyledons) under osmotic

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stress stress7. Hence, osmotic stress coordinates with seed size regulator AN3, large

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initial seed size, and increased fruit number, which determines the final large seeds of

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an3 mutants under osmotic stress.

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Abscisic acid-deficient 2 (ABA2)–ABA–abscisic acid-insensitive 5 (ABI5)–short

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hypocotyl under blue 1 (SHB1) signal transduction pathway

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ABA2–ABA–ABI5–SHB1

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signal-mediated seed size

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ABI5 is a basic region leucine zipper transcription factor. The RNA accumulation of

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ABI5 was observed in fruits by RT-qPCR analysis20, and Pro-ABI5:GUS is highly

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expressed in mature seeds, as described by the phenotype curated by ABRC. In

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addition, the lack of ABA2 (aba2) and the lack of ABI5 (abi5) generate large seeds

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by enlarged endosperms. And ABI5 modulates a subset of abundant genes of

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post-embryogenesis during seed development. On the other hand, SHB1

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overexpression presents increased seed size, and SHB1 can be expressed on

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endosperms and seed coat10. ABI5 binds directly to the SHB1 promoter and

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suppresses its expression to regulate seed size20. These findings indicate that ABA

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signaling and/or metabolism modulate seed growth by ABI5-mediated transcriptional

signal

transduction

pathway


to

control

ABA

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suppression of SHB1 in the endosperms20. Thus, under normal physiological

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conditions, these components form the ABA2–ABA–ABI5–SHB1 signal transduction

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pathway to control the ABA signal-mediated seed size (Figures 2 and 3).

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.

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ABA2–ABA–ABI5–SHB1 signal transduction pathway may be involved in ABA

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signal-mediated water-deficient tolerance

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Considering that the seedlings of large-seeded plants can withstand water-deficient

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stresses well11, and abi5 mutants presented large initial seed sizes20, if abi5 seedlings

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presented large seed sizes under water-deficient tolerance should be expored. The

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abi5 seeds in Arabidopsis reduce sensitivity to salt and osmotic stress during

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germination21, and stomatal aperture substantially increases through ABI5

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overexpression in the presence or absence of ABA under monochromatic light

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conditions; these light conditions are caused by BBX21 and a B-box transcription

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factor that directly binds to the ABI5 promoter for gas exchange when plants suffer

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from periodic water-deficient stress22. In addition, ABI5 is also involved in stomatal

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regulation23. These results suggested that abi5 mutant exhibits potential

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water-deficient tolerance. Further, abi5 mutant reveals increased fruit number and

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delayed meristem arrest, thereby resulting in prolonged life span25.

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The ABA2 promoter activity under prolonged stress conditions, including cold

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and drought, is enhanced24, thereby indicating that ABA2 may be involved in

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water-deficient tolerance regulation. In summary, the ABA2–ABA–ABI5–SHB1



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signal transduction pathway may be involved in ABA signal-mediated water-deficient

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tolerance (Figures 2 and 3). Together, though relative information has been reported,

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the tuning mechanism that water-deficient stress interacts with large initial seed size

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and increased fruit number in this pathway to determine final seed size should be

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further expored.

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GIGANTEA (GI)–miR172-FRUITFULL (FUL)–APETALA2 (AP2) signal

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transduction pathway

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GI mutation shows delaying flowering and promoting seed maturity or filling, thereby

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possibly forming large seeds under water-deficient stress

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Considerable reports showed that floral genes are involved in the coordination

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of flowering time with seed maturity/filling under water-deficient stress26. For

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example, under water-deficient stress condition, Arabidopsis flowering is accelerated

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during long days and delayed during short days. GI is related to photoperiodic

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flowering time that can accelerate flowering through the circadian and photoperiod

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pathways which are the important modulators of water-deficient escape response; for

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example, the lack of GI shows change in water-deficient escape responses27. Under a

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long-day condition, GI can promote the instability of the cycling DOF factor which is

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the repressor of the floral integrator genes FT and CO in terms of the transcriptional

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levels, thereby activating these integrators. GI also directly binds to the FT promoter

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to activate it28. Therefore, during long days, water-deficient stress induces the floral


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promoters TSF (the twin sister of FT) and FT in terms of the transcriptional levels

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which depend upon the GI manner, thereby accelerating flowering and likely

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decreasing seed maturity/filling. As a result, this condition may decrease the final

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seed size. At the same time, the plant stress hormone ABA is considerably induced

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under water-deficient stress27. Under a short-day condition, ABA and water-deficient

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stress are the repressors of floral promoter activation. As a result, these factors

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suppress ST and FT transcription27, thereby delaying flowering, promoting seed

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maturity or filling and forming large seeds. For example, several reports have

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suggested that the soybean genes of the photoperiodic flowering time or circadian

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regulate the development and maturity or filling of soybean seeds29-32. However, the

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relative mechanism is largely unknown and must be further researched.

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GI–miR172-FUL–AP2 pathway coordinates water-deficient stress with initial seed

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size and fruit number via sugar metabolism and/or ABA signalling to determine final

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seed size

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AP2 is a transcription factor belonging to the AP2/EREBP family3, and it can

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modulate the expression of stress-responsive genes33. The lack of AP2 (ap2) causes

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sugar signal-mediated large seed sizes due to abnormal embryo enlargement due to

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the increased seed integuments3. These results suggest that AP2 coordinating

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water-deficient stress with initial seed size may control final seed size of ap2 mutant

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via sugar metabolism and/or ABA signal pathway.

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FUL is a MADS-box gene that participates in flowering and fruit development,



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and it negatively and directly modulates AP2 expression to regulate meristem arrest

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and life span17. The lack of either FUL or AP2 increases fruit number, thereby

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delaying meristem arrest and prolonging life span17. In Arabidopsis, miR172

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positively regulates flowering by targeting SMZ and TOE2 of the AP2-like floral

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suppressors34,35. Also miR172 expression can be induced by water-deficient stress36

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and miR172 overexpression showed decreased fruit number and shortened life span17.

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However, whether miR172 regulates seed size remains to be determined. Together,

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water-deficient stress might affect on initial seed size/fruit number by sugar

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metabolism and/or ABA signalling mediated-GI–miR172-FUL–AP2 pathway to

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regulate final seed size (Figure 4). However, more evidences need be added to prove

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these concerns.

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IAA/ABA–auxin response factor 2 (ARF2)–AINTEGUMENTA(ANT)–COR15A

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signal transduction pathway

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ARF2 encodes transcription factors, and it mediates plant responses to the hormone

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auxin37. The lack of ARF2 (arf2) delays a few processes in plant senescence, such as

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flowering time, rosette leaf senescence, fruit ripening and floral organ abscission.

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These arf2 mutant lines also exhibited increased fruit number37, thereby delaying

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meristem arrest and prolonging life span. In addition, ARF2 negatively regulates seed

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size by controlling the cell division in the maternal integuments37. Thus, arf2 mutants

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produce ABA signal mediated-large seed size and increased fruit number (Table 1,


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Figure 5).

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ANT is a transcription factor in the AP2-domain family38. ARF2 directly binds

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to the ANT promoter and suppresses its expression, thereby positively regulating the

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seed size in Arabidopsis18. The loss-of-function mutant ant results in abnormal ovule

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and female gametophyte development and ABA signal-mediated small seed size as a

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result of abnormal embryo reduction due to the reduced seed integuments18,38. By

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contrast, ANT overexpression showed large seed size and delayed meristem arrest,

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thereby leading to prolonged life span18,39 and water-deficient tolerance caused by

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rapid stomatal opening and large root systems18. Thus, the overexpression of ANT

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results in ABA signal mediated-large seed size and increased fruit number (Table 1,

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Figure 5).

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Together, the IAA/ABA-ARF2-ANT pathway may be an integrated point of both

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water-deficient stress and initial seed size/fruit number to control final seed size

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(Table 1, Figure 5). However, further evidence be needed to confirm this concern..

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Involvement of few pathways related to seed size and fruit number regulation

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Involvement of GI–miR172–WRKY44/TTG2 pathway related to seed size and fruit

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number regulation

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In the GI–miR172–WRKY44/TTG2–glucose signaling pathway, Arabidopsis miR172

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promotes flowering by targeting the SMZ and TOE2 of the AP2-like floral



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suppressors34, and miR172 expression is induced by water-deficient stress36.

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Moreover, miR172 is involved in fruit number and life span regulation17. However,

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whether miR172 is involved in seed size regulation is unknown. The gene of

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WRKY44/TTG2 (TRANSPARENT TESTA GLABRA 2) is expressed in the seed

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integument and endosperm and positively regulates seed size8. WRKY44/TTG2 is

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participated

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GI-miRNA172-WRKY44/TTG2 may regulate either water-deficient tolerance or

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escape by influencing sugar signaling36. However, whether this pathway is involved

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in the regulation of fruit number and life span remains to be determined (Figure 4,

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Table 1).

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Involvement of SOD7–KLU pathway related to seed size and fruit number regulation

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In the SOD7–KLU pathway, the lack of SOD7 results in large seed sizes and early

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flowering40, whereas the lack of KLUH (KUL)/CYP78A5 exhibits small seed sizes

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and delayed flowering. Moreover, KUL/CYP78A5 is expressed at the periphery of the

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shoot apical meristem41. Further, SOD7 directly binds to the KUL promoter to

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suppress its expression for the regulation of seed size40. However, whether the fruit

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number and life span are regulated by the SOD7–KLU pathway under water-deficient

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stress remains unknown. Hence, the relative mechanism cross-talking this pathway

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with the initial seed size and fruit number to determine final seed size need be further

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researched

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Involvement of DA1–ubiquitin-specific protease 15 (UBP15) pathway relative to seed

in

sugar

signalling

and/or


metabolism.36

Therefore,

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size and fruit number regulation

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In the DA1–UBP15 pathway, DA1 is a ubiquitin receptor that controls the seed size

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by restricting cell division in maternal integuments42 and UBP15 functions

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considerably in promoting seed growth in Arabidopsis43,44. In details, the lack of

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UBP15 (ubp15-1) generates small seed sizes due to the decreased cell division and is

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epistatic to the lack of DA1 with regard to seed size43,44. And ubp15-1 also showed

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short roots at the seedling stage and aborted fruits, as indicated by the phenotype

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curated by ABRC. Further, DA1 interacts physically with UBP15 and modulates its

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stability, thereby indicating that DA1 is an upstream target of UBP15 in Arabidopsis.

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However, other relative information is largely unclear. Hence, the mechanism

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underlying the integration of DA1–UBP15 pathway into the initial seed size/fruit

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number to determine final seed size under drought stress should be expored.

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Involvement of MPK3/6 pathway relative to seed size and fruit number regulation

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According to few reports, large and small seed sizes are coordinated with

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water-deficient tolerance and sensitivity, respectively. For example, mitogen-activated

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protein kinase 3 and 6 (MAPK6) are the key modulators of stomatal development and

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patterning45. The double mutant of mpk3−/−/mpk6−/− of Arabidopsis shows

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considerably enhanced stomatal density or number45. Moreover, the lack of

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OsMAPK6 of rice generates small grains similar to those in smg1 mutants, and further

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OsMKK6 interacts physically with OsMAPK446, indicating the OsMKK6–OsMAPK4

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signal pathway controls rice grain size. Thus, the MPK3/6 pathway may coordinate



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water-deficient stress with the initial seed size to determine final seed size. However,

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how relative molecular mechanisms in details remains to be determined.

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Involvement of YDA pathway related to seed size and fruit number regulation

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Mutations in the gene encoding YDA which is a MAPKK kinase, can disrupt stomatal

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patterning and lead to clustered stomata that considerably increases stomatal density

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or index46. Simultaneously, the lack of YDA increases the embryo size and shortens

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root length7,18,48. As a result, the lack of YDA leads to decreased seed size and

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water-deficient sensitivity7. Enlarged root systems and decreased stomatal density can

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effectively tolerate water-deficient stress signalling caused by plant endogenous

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developmental signaling, thereby further indicating that endogenous developmental

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signaling coordinates with stress signaling18. Therefore, YDA may integrate

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water-deficient stress into the initial seed size to determine final seed size. However,

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relative molecular mechanism need be further expored.

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In summary, these regulatory pathways are the new insights into the mechanism

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underlying the integration of water-deficient stress signals into three genetic

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signalling factors (seed size regulators, initial seed size and fruit number), thereby

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indicating the mechanism underlying the effect of water-deficient stress on seed size.

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Conclusions and future perspectives are described as follows. Seed size is one of

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the most promising factors to consider in increasing the crop yield. Seed size can be

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dominantly controlled through environmental cues (especially water-deficient stress)

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and three genetic signals (seed size regulators, initial seed size and fruit number)3. In


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detail, water-deficient stress signaling is integrated into three genetic signals to

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determine final seed size, which may aid future design strategies or breeding to

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increase crop yield. Meanwhile, this approach may aid the preliminarily screening or

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identification of the novel genetic factors by identifying novel mutations and

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additional analysis of the known mutant lines under variable conditions. In the future,

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one of the major challenges is to elucidate the molecular mechanisms underlying the

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integration of water-deficient stress signaling into the pathways of three genetic

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signals in details, that is the identification of genetic frameworks. Scientists thus

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should also focus on the mechanism underlying the cross-talk of water-deficient

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tolerance with these traits because water-deficient stress is the most important factor

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in all environmental stresses. For example, identifying the genetic factors controlling

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fruit number and flowering time simultaneously controls seed size. Therefore, our aim

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is to study the new insights into the molecular mechanism that controls plant seed size

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under water-deficient stress.

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Acknowledgments

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This review benefited from grants from Natural Science Foundation of China

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(31770613; 31672148) and from Natural Science Foundation of JiangSu Province of

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China (BK20170236). The author declares no competing financial interest.

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Figure legend ACS Paragon Plus Environment


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Figure 1. In AN3-YDA pathway, three kinds of genetic signals (seed size regulators, the initial seed size, and fruit number) interact with water-deficient stress signaling to control final seed size. Blue fonts indicate three kinds of genetic signals. Under normal conditions, sugar promotes embryo cell elongation of an3 mutants. As a result, an3 mutant seeds contain additional protein and have large size5,7. When these an3 seeds are sowed, large seedlings are generated due to the large initial seed size. As comprehensively observed, the seedlings of large-seeded plants can considerably resist water-deficient stresses. In detail, an3 seedlings showed reduced stomatal conductance, reduced stomatal density, controlled MAPKKK, YDA, root elongation and increased lateral root number. As a result, an3 seedlings showed drought tolerance. By contrast, large an3 seedlings can increase the fruit number due to abnormal sugar levels. Figure 2. Water-deficient stress interacts with a few important signaling pathway to influence final seed size. Under

water-deficient

stress,

a

few

important

pathway

(SOD7-KLU,

DA1-UBP15,

IAA-ARF2-ANT-COR15A and ABA2-ABA-ABI5-SHB1) coordinates with initial seed size in Arabidopsis or other species.to control final seed size. Figure 3. In ABA2-ABA-ABI5-SHB1 signal transduction pathway, water-deficient stress signalling coordinates with three kinds of genetic signals (i.e. seed size regulators, initial seed size and fruit number) to control final seed size. Blue fonts indicate three kinds of genetic signals. Under normal conditions, abnormal ABA increases embryo cell number of abi5, aba2 and shb1-D mutants. As a result, abi5, aba2 and shb1-D mutant seeds contain additional protein and have large size. When these abi5, aba2 and shb1-D seeds are sowed, large seedlings are generated due to large size of initial seeds. As comprehensively observed, the seedlings of large-seeded plants can resist water-deficient stresses well. In detail, abi5 seedlings showed potentially increased ABA mediated-stomatal aperture. As a result, abi5 seedlings showed water-deficient tolerance. By contrast, large abi5 seedlings can increase fruit number due to abnormal ABA level.


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Figure 4. Water-deficient stress interacts with a few important signaling pathway to influence final seed size. Under water-deficient stress, a few important pathway (e.g. GI-miR172-WRKY44, AN3-YDA and FUL-AP2) coordinates with initial seed size in Arabidopsis or other species.to control final seed size. Figure 5. Water-deficient stress signaling coordinates with three kinds of genetic signals (e.g. seed size regulators, initial seed size and fruit number) in the ARF2-ANT-COR15A pathway. Blue fonts indicate three kinds of genetic signals. Under normal conditions, abnormal ABA promotes embryo cell number of 35S:ANT mutants. As a result, 35S:ANT mutant seeds contain additional protein and have large size. When these 35S:ANT seeds are sowed, large seedlings are generated due to large initial seed size. As comprehensively observed, the seedlings of large-seeded plants can resist water-deficient stresses well. In detail, 35S:ANT seedlings showed reduced stomatal conductance, rapid stomatal closing, ARF2-ANT-COR15A cascade formation, root elongation and increased lateral root number. As a result, 35S:ANT seedlings showed drought tolerance. By contrast, large 35S:ANT seedlings can increase fruit number due to abnormal ABA level. 312

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Table 1.

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Under water-deficient stress, a few important pathway (SOD7-KLU, DA1-UBP15, IAA-ARF2-ANT-COR15A and ABA2-ABA-ABI5-SHB1) coordinates with initial seed size in Arabidopsis or other species.to control final seed size.

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a TOC Graphic: Under water-deficient stress, a few important pathway (SOD7-KLU, DA1-UBP15, IAA-ARF2-ANT-COR15A and ABA2-ABA-ABI5-SHB1) coordinates with initial seed size in Arabidopsis or other species.to control final seed size.


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New insights into molecular mechanism underlying seed size control

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