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The Scaling Relationship of Below and Above-ground Biomass of Different Grain Crops during the Seedling Stage.

Byline: Xiaoliang Qin, Fengxia Zhang, Meiling Wang, Chengxiao Shi, Yuncheng Liao, Xiaoxia Wen and Kadambot H. M. Siddique

Abstract

Allometric partitioning theory showed that root biomass (MB) scales in a nearly isometric manner with respect to shoot biomass (MA) for natural plants. Artificial selection has fundamentally transformed plants; for example, the biomass allocation pattern has changed in grain crops. This study investigated 32 genotypes from 20 grain crop species to test the effects of domestication and seed size on the scaling relationship of MB vs. MA for grain crops. The scaling exponent of MB vs. MA during 30 days of growth was 0.937 across the 32 grain crop genotypes, 0.999 for the dicotyledons and 1.034 for the monocotyledons. Based on the 95% CIs of the MB vs. MA scaling exponent (aRMA) of the data sets for the 32 genotypes, eight values exceeded 1.0, nine values were less than 1.0 and the remaining 15 values were statistically indistinguishable from 1.0.

Seed size was positively correlated with the scaling exponents of MB vs. MA for the 32 genotypes (Pless than 0.05), which means large-seeded species generally had more potential for allocating biomass to roots during the seedling stage. These findings suggest that a uniform isometric relationship exists in grain crop species and that artificial selection in crop species has not changed this relationship. In addition, larger seeds are an evolutionarily-stable strategy based on high grain yield per area.

Keywords: Allometry; Breeding; Domestication; Seed size; Grain crop; Scaling exponent

Introduction

Interspecific relationships between below-and above-ground biomass (MB and MA, respectively) are used widely in studies on climate change, ecology and evolution; many of these size-dependent trends are considered a consequence of natural selection and adaptive evolutionary change (Wardlaw, 1990; Niklas, 1994; Bazzaz and Grace, 1997; Charnov, 1997; Tilman et al., 1997; Caspersen et al., 2000; Robinson et al., 2010). Allometric partitioning theory showed that MB scales in a nearly isometric manner with respect to MA across and within clades and different habitats (Enquist and Niklas, 2002; Niklas, 2005), and empirical statistical trends agree with this prediction (Niklas and Enquist, 2002; Enquist and Niklas, 2002; Niklas, 2004, 2005, 2006; Cheng and Niklas, 2007, Cheng et al., 2015).

Crop plants, including monocotyledons and dicotyledons, undergo both natural and artificial selection. Long histories of domestication, selection and breeding have fundamentally transformed plants (Cronquist, 1988; Evans, 1993). A series of changes has taken place in seed plants: the increased allocation of biomass to reproductive organs accounts for much of the progress in breeding for high yield potential in wheat, oat, barley, maize and sunflower (Slafer, 1994), along with more biomass being allocated to shoots in modern wheat genotypes (Siddique et al., 1990; Zhang et al., 1999, Qin et al., 2012) and that wheat and barley crops have larger seeds than wild types (Dubcovsky and Dvorak, 2007). Whether artificial selection has changed the uniform isometric relationship in grain crop species is unclear.

Seed size is central to many aspects of plant ecology and evolution (Harper et al., 1970; Leishman et al., 2000; Moles et al., 2005a, b; Sadras, 2007). Seed size may affect biomass allocation in an individual plant (Enquist and Niklas, 2002; Peng et al., 2010). Seed size is particularly significant at the seedling stage since germination is an important factor affecting crop yield, such that lower seed germination rates cause production losses. After seed germination, seeds with larger endosperms and cotyledons are more likely to develop larger MB/MA ratios than those with smaller endosperms and cotyledons (Khurana and Singh, 2000; Niklas, 2005), and have a survival advantage during seedling establishment (Moles and Westoby, 2004).

To represent genetic variation in grain crops around the world, we selected 32 genotypes from 20 major grain crop species (oil, cereal and legume crops), 11 of which were dicotyledons and nine were monocotyledons. Seed biomass of the 32 genotypes spanned two orders of magnitude (Fig. S1). We studied the allometric relationships of MB vs. MA during the seedling stage to test two hypotheses: (1) after long-term domestication by humans, MB does not scale in an isometric manner with respect to MA in grain crops, and (2) large-seeded genotypes allocate more biomass to roots during seedling growth.

Materials and Methods

Sixty grains of each genotype (Table 1) were selected, sterilized in 10% H2O2 for 30 min, repeatedly rinsed in distilled water until free of H2O2, and then incubated at 25C for 48 h. After accelerating germination, seedlings were transplanted to plastic pots (height, 25 cm; diameter, 20 cm) filled with moistened sand and vermiculite, and fertilized with half-strength modified Hoagland nutrient solution to prevent nutrient depletion (Hoagland and Arnon, 1950). Each pot contained three seedlings with 20 pots per genotype. The experiment was conducted in a growth chamber set at day/night temperatures of 25C/18C, relative humidity of 45/605%, photon flux density of 150 uM m-2 s-1 and a light period of 12 h.

Ten individual plants of each genotype were harvested on each of six harvest dates (5, 10, 15, 20, 25 and 30 days after sowing). Seedlings were removed with care, and roots carefully rinsed with running water until free of sand and vermiculite. Root and shoot dry weights were determined after oven drying for 30 mins at 100C followed by 48 h at 80C.

Data for MA and MB were log10-transformed and Model Type II (reduced major axis, RMA) regression analysis was used to determine the scaling exponents (aRMA) and allometric constants (log bRMA) (Niklas, 1994, 2005, 2006; Falster et al., 2006; Warton et al., 2006). The formula for the scaling equation is logMB = aRMA logMA + log bRMA.

The Standardized Major Axis Tests and Routines (MATR) software package (Warton and Weber, 2002; Falster et al., 2003) was used to determine if the numerical values of aRMA for log MA vs. log MB differed between contrasting data subsets. The formula for the scaling equation is logMB = aRMA logMA + log bRMA. Heterogeneity in the numerical value of either regression parameter was rejected for each comparison if P>0.05.

Results

The Scaling Relationship across Species

The scaling exponent of MB vs. MA during 30 days of growth was 0.937 (95% CIs = 0.918, 0.957; N = 1890; r2 = 0.793) across the 32 grain crop genotypes, which was near to 1.0. The scaling exponent for the dicotyledons was 0.999 (95% CIs = 0.977, 1.020; N = 940; r2 = 0.883) and the monocotyledons was 1.034 (95% CIs = 1.005, 1.063; N = 950; r2 = 0.816) (Figs. 1, 2 and 3).

The Scaling Relationship within Genotypes

Based on the 95% CIs of the MB vs. MA scaling exponent (aRMA) of the data sets for the 32 genotypes, eight values exceeded 1.0, nine values were less than 1.0 and the remaining 15 values were statistically indistinguishable from 1.0 (Table 2).

The Effect of Grain Size and Genotype on the Scaling Exponent of MB vs. MA

Tough points in Fig. 4 are slightly scattered, however seed size was positively correlated with the scaling exponent of MB vs. MA for the 32 grain crop genotypes (P=0.016).

Discussion

A normal rule of thumb for plants is that MB will scale in a nearly isometric manner with respect to MA across and within clades and different habitats (Enquist and Niklas, 2002; Niklas, 2005). Niklas (2005) conducted a study using a large database (1406 data entries for 257 species) and found that the scaling exponent for non-woody plants and juvenile woody species agreed reasonably well with an isometric scaling relationship. Specific variation in biomass allocation is well known in response to differential selection pressure. However, in our study with seed biomass across two orders of magnitude, MB scaled isometrically with MA for the dicotyledons, monocotyledons and across the 32 grain crop genotypes. The intergenomic allometric across the 32 grain crop genotypes was slightly lower than 1.0 which may be a result of maternal effects.

In other words, even though grain crop varieties have been selected for more than 10,000 years and a series of changes has taken place, the scaling allocation rules remain as per the natural plant.

Many of the intragenomic allometric scaling exponents (eight values exceeded 1.0, nine values were less than 1.0) were inconsistent with previous reports. However, the results do not conflict with an isometric relationship because roots are highly regulated by nutrient availability, and different crops may favor different soil conditions. In other words, the soil and nutrient levels proposed in the present study may be favored by some species, so the scaling exponent changed with species. Furthermore, at the seedling stage, the maternal effect of seed size is an important factor affecting biomass allocation in seedlings (Niklas, 2005). Our results showed that across two orders of magnitude for seed biomass, seed size and scaling exponent were positively correlated when 32 grain crop species were combined.

This means that large-seeded species are more likely to allocate biomass to roots than small-seeded species during seedling growth, which is useful for the germinating seed to absorb nutrients from the soil environment, particularly in poor soil (Palta et al., 2011).

Table 1: Details of the 32 genotypes of grain crop used in this study

Chinese genotype###Common name###Latin name###Application

Dicotyledons

Baiyundou###Kidney bean###Phaseolus vulgaris###Legume

Hongyundou###Kidney bean###Phaseolus vulgaris###Legume

Bima###Castor###Ricinus communis L.###Oilseed

Zaoshu 6###Soybean###Glycine max###Legume

Zhonghuang 13###Soybean###Glycine max###Legume

Hongxiaodou###Adzuki bean###Vigna angularis###Legume

LA1/4dou###Green bean###Vigna radiata (Linn.) Wilczek.###Legume

Meikui###Sunflower###Helianthus annuus###Oilseed

Sandaomei###Sunflower###Helianthus annuus###Oilseed

Jiujiangkuqiao###Tartary buckwheat###Fagopyrum tataricum (L.) Gaertn###Cereal

Tianqiao###Common buckwheat###Fagopyrum esculentum Moench###Cereal

Yuzhi8###Sesame###Sesamum indicum###Oilseed

Yuzhi4###Sesame###Sesamum indicum###Oilseed

Biandou###Lentil###Lens culinaris

Ganza 1###Rape###Brassica campestris L.###Oilseed

Jinyouza 2009###Rape###Brassica campestris L.###Oilseed

Monocotyledons

Liao5236###Corn(inbred line)###Zea mays###Cereal

LG001###Corn(inbred line)###Zea mays###Cereal

Luoyanmai###Naked oat###Avena nuda L.###Cereal

Aiganyanmai###Husk oat###Avena sativa###Cereal

Mazhamai###Wheat###Triticum aestivum L.###Cereal

Xinong979###Wheat###Triticum aestivum L.###Cereal

Ganpi 1###Barely###Hordeum vulgare L.###Cereal

Heisileng###Barely###Hordeum vulgare L.###Cereal

Saozhougaoliang###Sorghum###Sorghum bicolor L.###Cereal

Shandonghonggaoliang###Sorghum###Sorghum bicolor L.###Cereal

Longmi 7###Broomcorn millet###Panicum miliaceum L.###Cereal

Yumi 3###Broomcorn millet###Panicum miliaceum L.###Cereal

Hongjiugu###Foxtail millet###Setaria italica###Cereal

Jingu 27###Foxtail millet###Setaria italica###Cereal

Ezao18###Rice###Oryza sativa L.###Cereal

Linhan1###Rice###Oryza sativa L.###Cereal

Table 2: Summary of SMA regression parameters for the scaling relationships between root and shoot biomass at the seedling stage for the 32 tested crop genotypes; all relationships were highly significant (Pless than 0.001)

Group###n###r2###RMA###RMA

Dicotyledons

Baiyundou###60###0.696###1.343 (1.161, 1.554)###-1.491

Hongyundou###60###0.358###1.119 (0.908, 1.379)###-1.037

Bima###50###0.79###1.128 (0.988, 1.287)###-0.838

Zaoshu 6###50###0.859###1.426 (1.279, 1.589)###-1.884

Zhonghuang 13###60###0.73###1.616 (1.410, 1.852)###-2.308

Hongxiaodou###60###0.812###0.875 (0.781, 0.981)###-0.470

LA1/4dou###60###0.739###0.961 (0.840, 1.098)###-0.611

Meikui###60###0.615###1.124 (0.955, 1.322)###-1.090

Sandaomei###60###0.625###1.046 (0.891, 1.228)###-0.845

Jiujiangkuqiao###60###0.458###0.937 (0.773, 1.135)###-0.586

Tianqiao###60###0.519###0.804 (0.671, 0.964)###-0.295

Yuzhi8###60###0.363###0.993 (0.806, 1.223)###-0.588

Yuzhi4###60###0.431###1.122 (0.921, 1.366)###-0.837

Biandou###60###0.575###0.998 (0.842, 1.183)###-0.533

Ganza 1###60###0.701###1.210 (1.048, 1.396)###-1.194

Jinyouza 2009###60###0.614###1.362 (1.157, 1.602)###-1.320

Monocotyledons

Liao5236###60###0.942###0.945 (0.865, 1.024)###-0.143

LG001###60###0.911###0.998 (0.890, 1.011)###-0.314

Luoyanmai###60###0.832###1.045 (0.938, 1.164)###-0.248

Aiganyanmai###60###0.885###1.143 (1.046, 1.250)###-0.694

Mazhamai###60###0.904###1.036 (0.955, 1.124)###-0.196

Xinong979###60###0.833###1.015 (0.912,1.130)###-0.144

Ganpi 1###60###0.673###0.790 (0.680, 0.918)###-0.084

Heisileng###50###0.621###1.398 (1.172, 1.666)###-0.805

Saozhougaoliang###60###0.871###0.886 (0.807, 0.974)###-0.179

Shandonghonggaoliang###60###0.758###0.821 (0.722, 0.934)###-0.401

Longmi 7###60###0.837###0.734 (0.660, 0.816)###-0.084

Yumi 3###60###0.82###0.717 (0.642, 0.802)###-0.101

Hongjiugu###60###0.871###0.739 (0.672, 0.812)###-0.290

Jingu 27###60###0.792###0.655 (0.581, 0.738)###-0.125

Linhan1###60###0.715###0.874 (0.739, 1.010)###-0.171

Ezao18###60###0.600###0.847 (0.657, 1.037)###-0.135

Our results are consistent with previous findings in Albizia procera and 257 different species where larger seeds had more potential to develop larger MB/MA ratios (Khurana and Singh, 2000; Niklas, 2005).

Lower grain yields in the field often result from low survival and emergence rates. Large-seeded species, with larger embryos, suggest faster emergence and more competitive ability (Dalling and Hubbell, 2002; Moles and Westoby, 2004, 2006). Our results showed that large seeds also allocate more root biomass to seedlings, which is useful during seed emergence to absorb water and nutrients from the soil environment, and implies better seedling establishment. So sowing larger seeds is an evolutionarily-stable strategy based on high grain yield per area.

Conclusion

Our results suggested that (1) the interspecific isometric relationship between roots and shoots is constant even in a small data set of seedlings, (2) artificial selection in crop species has not changed this uniform relationship, and (3) the scaling exponent of MB vs. MA for 32 grain crops is approximately isometric. Our results confirmed that seed size had a maternal effect on biomass allocation, with large-seeded grain crops generally have higher scaling exponents which may lead to better seedling establishment.

The purpose of crop breeding is to improve grain yields. After years of domestication, the most obvious changes to crop species are the increased investment of biomass to reproductive organs and the reduced investment of biomass to the root system (Siddique et al., 1990). In future, it would be better to test our hypotheses over a whole growth period.

Acknowledgements

This work was supported by the National Key Technology Support Program (2015BAD22B03), the National Natural Science Foundation of China (Project No. 31401303) and the Special Fund for Agro-scientific Research in the Public Interest (201503121).

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