Magnesium Fertilizer-Induced Increase of Symbiotic Microorganisms

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Magnesium fertilizer-induced increase of symbiotic microorganisms improve forage growth and quality Jihui Chen, Yanpeng Li, Shilin Wen, Andrea Rosanoff, Gaowen Yang, and Xiao Sun J. Agric. Food Chem., Just Accepted Manuscript • DOI: 10.1021/acs.jafc.6b05764 • Publication Date (Web): 04 Apr 2017 Downloaded from http://pubs.acs.org on April 5, 2017

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Journal of Agricultural and Food Chemistry

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Magnesium fertilizer-induced increase of symbiotic

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microorganisms improve forage growth and quality

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Jihui Chen1, Yanpeng Li1, Shilin Wen2, Andrea Rosanoff3, Gaowen Yang1, Xiao Sun1*

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210095, PR China

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Hengyang 421001, PR China

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College of Agro-Grassland Science, Nanjing Agricultural University, Nanjing

Hengyang Red Soil Experimental Station, Chinese Academy of Agricultural Sciences,

Center for Magnesium Education & Research, 13-1255 Malama St., Pahoa, HI 96778,

USA

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*

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Tel & Fax:86-25-84399620.

To whom correspondence should be addressed. E-mail: [email protected],

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1

ACS Paragon Plus Environment


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Abstract

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Magnesium (Mg) plays important roles in photosynthesis and protein-synthesis;

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however, latent Mg deficiencies are common phenomena that can influence food

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quality. Nevertheless, the effects of Mg fertilizer additions on plant carbon (C):

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nitrogen (N): phosphorus (P) stoichiometry, an important index of food quality, are

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unclear and the underlying mechanisms unexplored. We conducted a greenhouse

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experiment using low-Mg in–situ soil without and with a gradient of Mg additions to

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investigate the effect of Mg fertilizer on growth and stoichiometry of maize and

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soybean, and also measure these plants’ main symbiotic microorganisms: arbuscular

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mycorrhizal fungi (AMF) and rhizobium, respectively. Our results showed that Mg

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addition significantly improved both plant species’ growth, and also increased N and

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P concentrations in soybean and maize, respectively, resulting in low C:N ratio and

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high N:P ratio in soybean, and low C:P and N:P ratios in maize. These results

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presumably stemmed from the increase of nutrients supplied by activation-enhanced

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plant symbiotic microorganisms, an explanation supported by statistically significant

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positive correlations between plant stoichiometry and plants’ symbiotic

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microorganisms’ increased growth with Mg addition. We conclude that Mg supply

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can improve plant growth and alter plant stoichiometry via enhanced activity of plant

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symbiotic microorganisms. Possible mechanisms underlying this positive plant–soil

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feedback include an enhanced photosynthetic product flow to roots caused by

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adequate Mg supply.

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Key words: magnesium, plant symbiotic microorganisms, plant growth and

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stoichiometry, maize, soybean

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Introduction

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Magnesium (Mg) is essential for the growth and development of plants, and plays an

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important role in photosynthesis because it is the central element of chlorophyll and is

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a cofactor of a series of enzymes involved in carbon fixation. Mg also plays a

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fundamental role in phloem export of photosynthates from source to sink organs such

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as roots.1 Latent and acute Mg deficiencies in plants are common phenomena because

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of its unique chemical property–a highly hydrated radius that sorbs less to colloids

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than other cations.2 Magnesium fertilizer not only increases plant photosynthesis by

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mitigating Mg deficiencies,3-7 but may also improve other nutrients’ uptake by root

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via enhancing transport of photosynthetic products to roots. Therefore, the

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physiological and biochemical changes caused by Mg fertilizer can not only increase

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plant growth, but may also alter plant stoichiometry which is a key characteristic trait

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that controls nutrients and energy transfer in food webs.8,9 Understanding the

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influence of Mg fertilizer on plant stoichiometry should thus provide important new

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information about physiological and ecological ramifications of mineral nutrients in

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terrestrial ecosystems. To our knowledge, no study has researched the influences of

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Mg fertilizer on plant stoichiometry, although such measurements can be very

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important for predicting plant-to-herbivore energy and nutrient flow.

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Ecological stoichiometry considers that all organisms are composed of the same

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major elements [carbon (C), nitrogen (N), and phosphorus (P)]. The balance of these

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elements as well as their supply affect consumers, and change of plant food

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stoichiometry measurements can provide perspective to predict the possible effects of

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fertilizer or other treatments on consumer animal growth.10 Studies of

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autotroph-herbivore interface (particularly for freshwater ecosystems) show that N or

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P fertilizer treatment changes plant C:N:P stoichiometry which then influences energy 3



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and mineral flow in these ecosystems.11-13 These studies found that food (plant) with

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moderate C : P and N : P ratios are most likely to result in efficient element trophic

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transfer, as excessively low or high C : P and N : P food (plant) ratios are not

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beneficial to growth of consumers (herbivores).11,13-15 Forage quality studies have

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generally focused on the contents of crude protein (a reflection of N content), but few

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studies have shown that Mg fertilizer enhanced protein content in food, and the

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underlying mechanism is unclear.7

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Mg fertilizer may enhance N and P acquisition by plant root via improving

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root growth and perhaps by enhancement of symbiotic microorganisms, which deliver

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limiting soil minerals (e.g. N and P) to their host plants in return for

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photosynthetically derived carbon.16-20 There is strong empirical evidence that Mg

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fertilizer results in dramatic increases in carbohydrate flow to roots,1,3,5 resulting in

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both enhanced root growth and enlarged contact area of root with soil.1,21-23

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Additionally, preferential partitioning of photosynthetic carbon to roots to increase

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limited elements’ uptake has also been reported.21,22 This increase of root

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carbohydrates caused by Mg fertilizer might also enhance the mutualistic interactions

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between host plant and microbes such as arbuscular mycorrhizal fungi (AMF) in

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grasses and rhizobium in legumes. With Mg fertilizer, this increase of both root

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growth and plant mutualistic microorganisms could together enhance the nutrient and

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water acquisition by roots, perhaps altering plant growth as well as C:N:P

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stoichiometry.23

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In the current study, a greenhouse experiment was conducted to investigate

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the effects of Mg fertilizer in low Mg soil on forage maize and soybean growth and

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stoichiometry. The influence of Mg fertilizer on colonization of these plants’

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mutualistic microorganisms was also evaluated. We hypothesized that: 4


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(i) Mg addition in both species would improve plant growth and activate plant mutualistic microorganisms; (ii) Mg addition would enhance N, P and Mg concentrations in leaves (resulting in decreased C:P and C:N ratios) in both species; (iii) Mg addition would bring no change in N:P ratio in maize (a grass) but

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would increase N:P ratio in soybean (a legume) due to different properties of

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arbuscular mycorrhizal fungi and rhizobium.

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Materials and methods

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Experimental design

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Acid red-yellow soil in south is usually poor in Mg because of soil acidification and

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leaching due to high precipitation, and plants in this soil also suffer from P deficiency.

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Therefore, we collected the acid red-yellow soil from Hengyang Red Soil

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Experimental Station in Hunan province, and mixed for homogeneity. The five mixed

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soil samples were air-dried in a shaded and ventilated environment for approximately

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one month to achieve a constant weight for determination of soil pH and total

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elements. The soil total N, P, available Mg, and organic carbon concentrations and pH

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were 0.082%, 0.036%, 0.0015%, 1.33% and 4.3, respectively.

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A total of 50 plastic pots (20 cm in diameter, 24 cm in depth) were filled with

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the well-mixed soil, each pot containing 4 kg soil. The soil-filled pots were then

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divided into two groups of 25 pots per group, resulting in 25 pots for each of the two

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species (maize or soybean). As done on previous studies conducted at this site, we set

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5 treatments of Mg addition (0, 20, 50, 100 and 200 mg kg-1 MgCO3) for each group

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(one species) with 5 replications. The total MgCO3 fertilizer (powder) was calculated

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according to each treatment concentration and soil weight.

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Plant materials

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Maize and soybean were selected as model species for close relationships with AMF

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and rhizobium, respectively. At the beginning of May, ~10 maize or soybean seeds

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were sown in each pot in the greenhouse. We watered the seedlings every other day,

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and the water level was adjusted using an electronic weigher once every three days to

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keep similar soil moisture content. The pot position was also changed randomly once

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every three days to avoid light heterogeneity. After three weeks, the seedlings (~10

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cm) were thinned in each pot to allow sufficient space for seedling growth with 3

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similar seedlings kept in each pot. We gently removed the upper soil (~2 cm) from

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free room in each pot, and then evenly sprinkled corresponding MgCO3 and recovered

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using “the removed upper soil”. After fertilization, we evenly sprinkled water to help

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plant uptake.

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Sampling and chemical analysis

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After 8 weeks, we harvested the plants. All plants were divided into roots and shoots.

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The roots were cleaned with tap water and then ultrapure water, and finally blotted

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dry with superabsorbent paper. One-tenth of fresh roots of maize were used for

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measuring AMF colonization (see below). The root nodules of soybean were removed,

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counted, and weighed using ten-thousandth analytical electronic balance after blotting

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dry with superabsorbent paper. These weights and numbers of soybean nodules were

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used to quantify the degree of rhizobium colonization. To measure chlorophyll

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content, about 2 g mature fresh leaves were extracted with 80% (v/v) acetone, and

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chlorophyll was measured using spectrophotometry.24 Remaining parts of plant

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samples and nodules were oven-dried at 65℃for 72 h. The nodules, shoots and roots

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(without rhizobium nodules) were cooled to room temperature in a desiccator and

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were weighed to determine dry biomass. Leaves and stems were then separated for 6


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each shoot; only mature dried leaves were used for elemental analysis and

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stoichiometry calculations. In preparation for chemical analyses, all plant samples

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were ground in 20-inch mesh in Wiley Mill. All samples were kept cool and dry for

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chemical analysis.

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AMF colonization: The roots used to measure AMF colonization were cut into

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approximately 1-cm lengths and were cleared in 10 % (w/v) KOH at 90 °C in a water

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bath for 30 min, then washed and stained with 0.05 % (w/v) Trypan blue developed

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by Trouvelet (1986).25 Using a dissection microscope, thirty root segments of each

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sample were assessed for percentage of root length colonized by AMF.

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Elemental analyses of leaf samples: Dried mature leaf samples were analyzed for total

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C and N concentrations (mg g-1) utilizing an elemental analyzer (Vario EL III,

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Elementar, Germany) and for P and Mg using an inductively coupled plasma emission

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spectrometer (Iris Advantage 1000, USA) once the samples were digested using

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trace-metal-grade nitric and perchloric acid, which was diluted in 100 ml of double

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distilled water.

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Statistical analysis

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The data were log-transformed when necessary to meet the parametric test

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assumptions of normality (Bartlett test) and homogenous variances, and then one-way

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ANOVA was used to determine the effects of Mg treatment on plant growth, leaf

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stoichiometry, and colonization rate of AMF and rhizobia. If data after transformation

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did not meet the parametric test assumptions of normality, the Kruskal-Wallis test was

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used. Pearson's product-moment correlation was used to analyze the relationships

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among plant growth, leaf stoichiometry and plant symbiotic microorganisms. Data

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analyses were performed with R 3.0.2 (R Development Core Team 2005).

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Results

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Effects of magnesium fertilizer on leaf chlorophyll and plant growth

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Total chlorophyll, chlorophyll a and chlorophyll b concentrations in mature leaves

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were significantly increased by Mg addition in both species, at >50 mg kg-1 addition

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level in maize and >20 mg kg-1 Mg addition for soybean (Figure 1). Mg fertilizer

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showed no significant influence on shoot biomass of maize, but significantly

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increased the shoot biomass of soybean (Figure 2a). The root biomass of both species

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increased with low Mg additions (20 or 50 mg kg-1 MgCO3) while high Mg addition

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(100 – 200 mg kg-1 MgCO3) showed no effects (Figure 2b). Low Mg addition (20 mg

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kg-1 MgCO3) showed no effects on total biomass, whereas, moderate (50 mg kg-1 or

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100 mg kg-1 ) Mg additions had significant positive effects on total biomass while

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high Mg additions had no further positive effect (Figure 2b and c).

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Effects of magnesium fertilizer on plant mutualistic microorganisms

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Except for low Mg treatment levels (20 or 50 mg kg-1 MgCO3 ), Mg treatment up to

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100 mg kg-1 significantly increased AMF colonization in maize, and the effect of

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further additional Mg (at high Mg treatment 200 mg kg-1) showed no further

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improved effect (Figure 3a). The rhizobium showed a similar pattern to AMF with Mg

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addition, reflected in both high nodulation and total nodule weight of each plant in

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response to Mg addition (Figures 3b and c).

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Effects of magnesium fertilizer on plant stoichiometry

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The dry leaf Mg concentration of both species significantly increased with Mg

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addition (Figure 4), while there was no significant change of C concentration (data not

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shown in Figure 4). Mg addition showed no significant effects on N concentration in

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maize leaf, except at the highest level of Mg addition which significantly decreased N

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concentration. In contrast, all levels of Mg addition >20 mg kg-1 showed a significant 8


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increase of N in soybean leaf. Mg addition, except at the highest level (200 mg kg-1),

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significantly increased P concentration in maize leaf, whereas there was no significant

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influence of Mg treatments on P in soybean leaf, except at the highest level of Mg

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addition, which significantly decreased P concentration (Figure 4).

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All levels of Mg addition reduced N:P ratio significantly in maize leaf (Figure.

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4), but Mg addition at levels >20 mg g-1 significantly enhanced N:P ratio in soybean

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leaf. Furthermore, the N:P ratio in maize leaf was reduced similarly at all levels of Mg

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addition (20 to 200 mg kg-1 MgCO3) (Figure 4). In contrast, Mg addition of 50 and

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100 mg kg-1 MgCO3 doubled leaf N:P ratio, and 200 mg kg-1 Mg addition further

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increased leaf N:P of soybean leaves significantly and substantially another 40%

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(Figure 4). The C:N ratio in soybean leaves significantly decreased with Mg addition

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except for 20 mg kg-1 MgCO3, whereas, there were no significant influences on C:N

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ratio in maize leaves (Figure 4). Mg addition decreased C:P ratio in maize leaves with

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no difference between treatments, but showed no influence on C:P ratio in soybean

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leaves except for a significant increase at the highest level of Mg addition (Figure 4).

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Relationships of plant biomass or stoichiometry with symbiotic microorganisms

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The average weight and number of individual plant rhizobium nodules showed

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significant positive correlation with both plant biomass and mature leaf N

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concentration (resulting in negative relationships between weight of rhizobium and

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C:N ratio, and positive relationships with N:P ratio) (Table 1). By contrast, the AMF

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colonization showed no significant relationships with plant biomass and measured

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elements in mature leaf, but did show a significant negative relationship with N:P

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ratio (Table 2).

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Discussion

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Influences of magnesium fertilizer on plant growth

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As in recent studies,6,7 appropriate Mg fertilizer significantly increased chlorophyll

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content in both maize and soybean, reflecting an increase of photosynthesis under Mg

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fertilizer conditions. Similar to some previously reported findings that Mg fertilizer

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increased plant biomass,1,6,7,26 we found that shoot, root and total biomass increased in

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soybean with Mg addition while in maize only root and total biomass increased. A

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few studies also have observed no effects of Mg fertilizer on biomass of shoot.6,27-29

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These inconsistent results may be due to different physiological and biochemical

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responses of plants and their symbiotic microorganisms to Mg addition.6,29,30 The

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positive effects of moderate Mg addition on root growth were not seen in either

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species under high Mg addition conditions. Perhaps this reflects allocation of more

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photosynthetic C to root mutualistic microorganisms rather than to root growth as a

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more efficient mode of nutrient acquisition. This interpretation was supported by high

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AMF colonization in maize and increased ratio of root nodule biomass:root biomass

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in soybean with Mg addition (Figure S1).

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Colonization of plant mutualistic microorganisms in response to magnesium

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fertilizer

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Rhizobium: As expected, Mg-treated soybean plants had more and larger nodules.

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Similar results were reported by Kiss et al (2004),27 and they considered that Mg has

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an important role in the metabolism of the rhizobium bacteria and nodule

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development, because (N2)-fixing rhizobium strains need ATP that must be present as

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a Mg-complex.27 Another possible contributing mechanism for the positive influence

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of Mg addition on rhizobium bacteria may be the increase of carbon flow to root

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induced by Mg addition,1 making more nutritional C available to rhizobium for 10


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growth. Although we did not find a significant increase of sugar in roots under Mg

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addition (except for low Mg addition) to support this interpretation, this may be

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because we only measured the sugar in the roots without nodules. This needs to be

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tested.

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AMF: As found here, a previous study showed that Mg addition has a pronounced

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positive effect on root AMF infection of maize, a result that could not be explained by

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changes in pH or osmotic pressure of the nutrient solution.28 Conversely, a few other

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studies reported an inhibitory effect of Mg fertilizer on colonization of mycorrhiza

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fungi.31,32 These inconsistent results may arise from an imbalance of Mg and other

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elements, such as Ca, which can disrupt the mycorrhizal association with its host plant,

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or differences of bacterial strain.31,32 Here, we also suggest that the increase of

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mutualistic association was attributable to the enhanced phloem export of sucrose

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under Mg addition conditions (Figure S2).

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Plant stoichiometry in response to magnesium fertilizer

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Nitrogen: As our hypothesis predicted, Mg addition doubled N (or protein)

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concentration in soybean leaf, presumably as a result of the increase of biological

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nitrogen fixation in larger and more numerous root nodules. In contrast, there was no

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rise and even a slight decrease in maize leaf N concentration with Mg addition, a

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possible “dilution effect” due to the increase of biomass. These results suggest that

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Mg fertilizer may improve protein content in legume-based food as much as nitrogen

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fertilizer,33 or reduce protein in grass-based food while raising leaf P as might a

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phosphorus fertilizer34 albeit with different mechanisms. The different responses of

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the two species can be attributed to the different biochemical roles of their main

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symbiotic microorganism, i.e. rhizobium and AMF, as it is generally known that

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rhizobium can fix nitrogen from the atmosphere while AMF mainly delivers various 11



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soil mineral elements, especially P.

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Phosphorus: These functional differences in microorganisms may also explain

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differences in the total P content of the two species’ responses to Mg treatments and

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the marginally significant increase of P in maize leaves with Mg addition not seen in

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soybean leaves.

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Magnesium: In previous studies, as in the present study, Mg treatments significantly

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increased Mg concentration in leaf,6 which can be beneficial to animal nutrition in

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decreasing35 the risk of grass tetany of herbivores36 and in plant foods destined for

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human consumption which have shown decreased Mg concentration over time,

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especially with the high yield cultivars.37

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C:N:P Ratios: The C:N ratio in leaf of Mg-treated soybean was 50% lower than in

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non-treated soybean leaf; by contrast, soybean leaf N:P ratio more than doubled with

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Mg treatment. This is primarily due to the increase of symbiotic N fixation seen in

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Mg-treated soybean. The decrease of C:P and N:P ratios in maize leaf with Mg

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addition was associated with an increase of leaf P. According to theories behind

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stoichiometry studies, decreased C:N (seen in our soybean plants with Mg addition)

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or C:P (seen in our maize plants with Mg addition) ratios in plants may improve C

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flow to herbivores.10 Significant correlations between stoichiometry and mutualistic

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microbes in this study suggest that the differences in leaf C: N : P stoichiometry

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between maize and soybean come primarily from their differing mutualistic

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interactions between plant and microbe that are enhanced by Mg fertilizer.

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Conclusions

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Our results suggest that moderate Mg fertilization improved plant growth and altered

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C:N:P stoichiometry primarily via enhancement of mutualistic interactions between

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host plant and microbes as well as by promoting root growth. The potential 12


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mechanisms underlying this positive effect of Mg addition include an enhanced

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photosynthetic production flow from source leaves that promotes root growth and

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“feeds” mutualistic microbes, and, possibly, a direct, positive Mg effect on AMF and

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rhizobium development that delivers more nutrients to the host plants. Such change of

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stoichiometry brought about by Mg addition may favor nutrient and energy transfer in

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food webs. Our study has important implications for understanding the influence of

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Mg fertilizer and its underlying mechanisms on plant quality, and contributes

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information for farmland management strategies that could improve food quality and

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yield.

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Acknowledgments

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We thank Shuijing Hu for helpful suggestion on the experiment, and Christina West

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for proofreading the manuscript. This work was financially supported by National

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Natural Science Foundation of China (NSFC 600030), Basic research program of

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Jiangsu province (Natural Science Foundation) -Youth Foundation (BK20150665),

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and Student Research Training Program (1526A01).

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Supporting Information Available: [Methods of soluble carbohydrate analyses;

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Results of rhizobium nodule to root biomass ratio in soybean with Mg addition (Fig.

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S1); Soluble carbohydrate in leaf and roots of maize and soybean under Mg addition

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(Fig. S2).] This material is available free of charge via the Internet at

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http://pubs.acs.org.

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Figure Captions

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Figure 1 The effect of magnesium addition (20, 50, 100, and 200mg kg-1 MgCO3) to

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acid red-yellow (low Mg) soil on total chlorophyll (a), chlorophyll a (b) and

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chlorophyll b (c) in maize and soybean leaves. Different letter (capital for maize and

423

lowercase for soybean) indicate significant differences between treatment means

424

(Student-Newman-Keuls test, p< 0.05).

425

Figure 2 The influence of magnesium additions (20, 50, 100, and 200mg kg-1 MgCO3)

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to acid red-yellow (low Mg) soil on shoot (a) and root biomass (b), and shoot:root

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biomass ratio (c) in maize and soybean. Different letter (capital for maize and

428

lowercase for soybean) indicate significant differences between treatment means

429

(Student-Newman-Keuls test, p< 0.05).

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Figure 3 The effect of magnesium additions (20, 50, 100, and 200mg kg-1 MgCO3) to

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acid red-yellow soil on

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rhizobium in soybean. Different letter indicate significant differences between

433

treatment means (Student-Newman-Keuls test, p< 0.05).

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Figure 4 Nitrogen (N), phosphorus (P), magnesium (Mg) concentrations and carbon

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(C):N:P ratios in leaves of maize and soybean under different magnesium additions

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(20, 50, 100, and 200mg kg-1 MgCO3) to acid-red-yellow soil. Different letter (capital

437

for maize and lowercase for soybean) indicate significant differences between

438

treatment means (Student-Newman-Keuls test, p< 0.05).

infection rate of AMF (a) in maize roots and (b, c)

19



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Table 1 Results of Soybean relationships (Pearson’s product-moment correlation)

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among shoot biomass (SB), leaf stoichiometry, and its symbiotic microorganisms.

441

The*, and ** represent significance at α = 0.05, and 0.01, respectively, and * indicate

442

marginal significance (0.06>α > 0.05). Characteristic TNR Chl TWR 0.89* 0.91* TNR 0.82 Chl SB N P C:N C:P

SB 0.88* 0.98** 0.87*

N 0.98** 0.94* 0.86* 0.90

P -0.0008 -0.39 -0.13 -0.41 -0.18

C:N -0.98** -0.9* -0.86 -0.86 -0.995** 0.11

C:P 0.31 0.66 0.38 0.65 0.48 -0.95* -0.42

N:P 0.91* 0.97** 0.83 0.93* 0.98** -0.38 -0.96** 0.65

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Note TWR= average total weight of nodules/plant, TNR = average total number of rhizobium

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nodules/plant, ChI, Chlorophyll, N nitrogen, P phosphorus, C carbon.

445

20


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446

Table 2 Results of Maize relationships (Pearson’s product-moment correlation)

447

among shoot biomass (SB), leaf stoichiometry, and its symbiotic microorganisms. The

448

* and ** represent significance at α = 0.05, 0.01, respectively. Characteristic Chl AMF 0.99** Chl SB N P C:N C:P

SB 0.83 0.89*

N -0.71 -0.69 -0.80

P 0.56 0.61 0.31 0.12

C:N 0.61 0.60 0.76 -0.99** -0.22

C:P -0.71 -0.74 -0.46 0.11 -0.97** -0.01

N:P -0.94* -0.96* -0.80 0.62 -0.71 -0.53 0.85

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Note AMF arbuscular mycorrhizal fungi, N nitrogen, P phosphorus, C carbon, and bold letters

450

indicate significant relationships (p

Magnesium Fertilizer-Induced Increase of Symbiotic Microorganisms

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