Effect of elevated carbon dioxide on plant biomass and grain protein concentration differs across bread, durum and synthetic hexaploid wheat genotypes

Highlights

• Genotype is a greater determining factor for grain protein concentration decline under elevated CO₂ than wheat type.

• Most genotypes declined in grain protein concentration under elevated CO₂, while increasing in total grain protein.

• Elevated CO₂ leads to a different response of harvest index between tetraploid and synthetic hexaploid genotypes.

• Biomass dilution is not the sole cause of grain protein concentration decline under elevated CO₂ in wheat.

Abstract

Atmospheric carbon dioxide conditions predicted for future climates cause increases in wheat biomass, but also decreases wheat grain protein concentration. We investigated the response of grain protein concentration of wheat to elevated carbon dioxide in nineteen wheat genotypes, including five tetraploid, eleven hexaploid and three synthetic hexaploid genotypes to test whether decreased grain protein is genotype dependent and whether it is caused by biomass dilution. These were grown in ambient and elevated carbon dioxide conditions simultaneously. Shoot biomass and grain samples were taken at maturity. The grain protein concentration, grain biomass, shoot biomass and harvest index were analysed for each genotype. Despite most genotypes increasing in total grain protein (g), the majority of genotypes decreased in grain protein concentration (%) under elevated carbon dioxide. Elevated carbon dioxide caused an increase in grain biomass for all genotypes and total shoot biomass for most genotypes, with harvest index increasing for all genotypes except the two synthetic hexaploids CPI133814 and CPI133811. Most of the differences between wheat types were not statistically significant, suggesting that the individual genotype of wheat plants determines the response to elevated carbon dioxide rather than the wheat type.

Introduction

One of the main components of global climate change is the increasing concentration of carbon dioxide (CO₂) in the atmosphere. Under future climates, the increased atmospheric CO₂ concentration ([CO₂]) will directly affect the yield, growth and development of crop plants (Ainsworth and Long, 2005; Leakey et al., 2009). For wheat (Triticum aestivum), although elevated [CO₂] (e[CO₂]) usually improves plant biomass and grain yield (Thilakarathne et al., 2013), the nutritional aspects of the grain suffer the opposite effect, where the concentration of protein and many macro and micronutrients declines (Fernando et al., 2012). With the global human population expected to increase, there will be a greater demand on food production. As such, the effect of climate change on food crops is of great concern.

Wheat is one of the most important food crops in the world, accounting for nearly a third of the global cereal production in the 2015/2016 season (FAO, 2017). Wheat species typically belong to three different ploidy levels, consisting of diploids (2n = 2x = 14), tetraploids (2n = 4x = 28) and hexaploids (2n = 6x = 42). The hexaploid wheat genome is comprised of seven pairs of chromosomes each in three genomes, called the A, B and D genomes. Hexaploid wheat was created from the hybridisation of the tetraploid T. turgidum (containing the A and B genomes) with the D donor Aegilops tauschii (Matsuoka, 2011). Synthetic hexaploid wheat is created by hybridising these two species, followed by amphidiploidisation (Yang et al., 2009). With this method, breeders are able to develop synthetic hexaploid wheat genotypes which incorporate genes from T. turgidum and Ae. tauschii that were not maintained during hexaploid wheat evolution, including traits such as drought tolerance (Reynolds et al., 2007), increased nutrient uptake (Calderini and Ortiz-Monasterio, 2003) and pathogen resistance (Wang et al., 2016). These synthetic hexaploids can then be crossed with bread wheat cultivars to transfer across the elite genes and improve upon the bread wheat cultivar (Li et al., 2014).

Growth under e[CO₂] causes increased yields in wheat (Amthor, 2001; Högy et al., 2009), but many studies have shown that it also causes a decline in nitrogen stored in the grain at maturity (Taub et al., 2008; Högy et al., 2013; Fernando et al., 2015). Protein composition of wheat grain grown under e[CO₂] is also affected, resulting in lower bread making quality in some cultivars (Fernando et al., 2015). Of the proteins in the grain, storage proteins (glutens), rather than structural or metabolic proteins, appear to be the most affected by e[CO₂] (S. Arachchige et al., 2017).

Previous studies have looked at the effect of e[CO₂] across diploid, tetraploid and hexaploid wheat species (Sinha et al., 2009; Uprety et al., 2009). Uprety et al. (2009) observed that the responses of each species to e[CO₂] was different depending on the physiological variable measured. For example, variables such as photosynthesis, leaf area, dry weight, grain yield and harvest index (HI) had a greater response to e[CO₂] in hexaploids and tetraploids than diploids. Sinha et al. (2009) also found differing responses of each ploidy level for their variables studied. Protein concentration in grains decreased for all ploidy levels, though the decrease was lowest in tetraploids and highest in hexaploids. How synthetic wheat responds to e[CO₂] has not previously been determined.

A major goal for wheat breeders has been to develop cultivars with improved HI. As such, identifying wheat with a high HI is important for the continual improvement of commercial wheat cultivars. Elevated [CO₂] increases both the grain yield (Amthor, 2001) and shoot biomass (Kimball, 2016) of wheat, with the ratio of these two components determining the plant's HI. The stimulation of both biomass and yield at the same magnitude can lead to no change in HI, which has been seen in both hexaploid bread wheat and tetraploid durum wheat (Wang et al., 2013; Aranjuelo et al., 2015; Fitzgerald et al., 2016). Furthermore, some studies have shown HI to both increase and decrease in some wheat cultivars (Uddling et al., 2008; Wang et al., 2013). Thilakarathne et al. (2013) found that increases in grain yield are associated with increases to leaf mass area due to e[CO₂]. As such, the degree that e[CO₂] increases grain yield, and in turn HI, may rely partly on how leaf mass area is affected. Increased HI, however, may lead to decreased grain protein concentration (GPC) in wheat due to dilution of N with increased carbohydrates (Taub et al., 2008).

In this study, we aimed to identify whether the effect of e[CO₂] on wheat GPC is dependent on wheat type and whether GPC decline is affected by HI and/or biomass dilution. We also investigated how e[CO₂] affects the GPC of synthetic hexaploid wheats. To achieve these aims we grew nineteen wheat cultivars under e[CO₂] and a[CO₂], consisting of five tetraploid, eleven hexaploid and three synthetic hexaploid genotypes, and analysed their biomass and protein content. One-Way ANOVA analysis was used to determine the significance of [CO₂] on the traits measured in the study.