Arabidopsis Type III Gγ Protein AGG3 Is a Positive Regulator of Yield and Stress Responses in the Model Monocot Setaria viridis

Abstract

Heterotrimeric G-proteins are key regulators of a multitude of growth and development pathways in eukaryotes. Along with the conserved G-protein components found in all organisms, plants have certain novel variants with unique architecture, which may be involved in the regulation of plant-specific traits. The higher plant-specific type III (or Class C) Gγ protein, which possesses a large C terminal extension, represented by AGG3 in Arabidopsis, is one such variant of canonical Gγ proteins. The type III Gγ proteins are involved in regulation of many agronomically important traits in plants, including seed yield, organ size regulation, abscisic acid (ABA)-dependent signaling and stress responses, and nitrogen use efficiency. However, the extant data, especially in the monocots, present a relatively complex and sometimes contradictory picture of the regulatory role of these proteins. It remains unclear if the positive traits observed in certain naturally occurring populations are due to the presence of specific allelic variants of the proteins or due to the altered expression of the gene itself. To address these possibilities, we have overexpressed the Arabidopsis AGG3 gene in the model monocot Setaria viridis and systematically evaluated its role in conferring agriculturally relevant phenotypes. Our data show that AtAGG3 is indeed functional in Setaria and suggest that a subset of the traits affected by the type III Gγ proteins are indeed positively correlated with the gene expression level, while others might have more complex, allele specific regulation.

Control of grain size by G protein signaling in rice

“…In addition, plant G proteins play the conserved function in the regulation of seed/grain size. For instance, G proteins in Arabidopsis , Setaria , Hordeum , and Camelina also regulate seed size (Chakravorty et al ; Li et al ; Roy Choudhury et al ; Wendt et al ; Kaur et al ). Thus, further studies about G protein‐mediated regulation of rice grain size and yield would be beneficial for yield improvement in other key crops.…”

The Role of Gβ Protein in Controlling Cell Expansion via Potential Interaction with Lipid Metabolic Pathways

“…Other G-protein subunits such as the Ga proteins in maize, and Ga and Gg proteins in rice, wheat (Triticum aestivum), barley (Hordeum vulgare), and Camelina have been shown to influence yield traits by directly affecting seed size, seed number, ear size, panicle branching and erectness, nitrogen use efficiency, etc. (Botella, 2012;Roy Choudhury et al, 2014;Sun et al, 2014Sun et al, , 2018Alvarez et al, 2015;Wendt et al, 2016;Xu et al, 2016;Kaur et al, 2018;Liu et al, 2018). This combined with their effect on biotic and abiotic stress responses, water use efficiency, and overall plant adaptation suggests that G-proteins will be a major target of future targeted breeding practices to improve plant yield.…”

“…The most elaborate data are available from Arabidopsis where G-protein mutants exhibit altered phenotypes in response to almost all plant hormones at the physiological and molecular (large-scale omics) level (Pandey and Assmann, 2004;Pandey et al, 2006Pandey et al, , 2008Pandey et al, , 2009Pandey et al, , 2010Fan et al, 2008;Zhao et al, 2010;Alvarez et al, 2011;Chakravorty et al, 2011;Jin et al, 2013;Tsugama et al, 2013;Wang et al, 2017;Peng et al, 2018;Zhang et al, 2018b). Similarly, G-protein mutants in Arabidopsis (and other plants) show altered sensitivity to multiple abiotic stresses such as drought, temperature, salt, redox, ultraviolet, and high light (Zhang et al, 2011;He et al, 2013;Torres et al, 2013;Subramaniam et al, 2016;Lee et al, 2017;Kaur et al, 2018;Yu and Assmann, 2018). G-proteins also mediate regulation of defense responses against host and nonhost bacterial pathogens, a variety of biotrophic and necrotrophic fungi and viruses (Liu et al, 2013;Lorek et al, 2013;Aranda-Sicilia et al, 2015;Cheng et al, 2015;Maruta et al, 2015;Meng et al, 2015;Liang et al, 2016Liang et al, , 2018Yuan et al, 2017;Bi et al, 2018;Wang et al, 2018).…”

“…All G-protein mutants exhibit skotomorphogenetic phenotypes during seedling development; there are clear differences in their shoot apical meristem development, leaf shape, stomatal density, root mass, and overall architecture (Ullah et al, 2003;Chen et al, 2006;Zhang et al, 2008;Bommert et al, 2013;Wu et al, 2018). Moreover, a subset of plant-specific, Cys-rich Gg proteins (Type III Gg) control reproductive organ size, seed size, seed number, and flowering time (Chakravorty et al, 2011;Li et al, 2012;Roy Choudhury et al, 2014;Wendt et al, 2016;Vavilova et al, 2017;Kaur et al, 2018;Sun et al, 2018). Finally, quantitative trait loci analyses have identified specific G-protein subunits responsible for branching, panicle erectness, panicle density, grain size, and nitrogen use efficiency in rice, emphasizing their direct relevance for affecting important agronomic traits (Huang et al, 2009;Mao et al, 2010;Sun et al, 2014Sun et al, , 2018Wendt et al, 2016;Xu et al, 2016;Vavilova et al, 2017).…”

Mutation of RGG2, which encodes a type B heterotrimeric G protein γ subunit, increases grain size and yield production in rice

“…AGG3 was the last identified G c subunit in Arabidopsis, and it has been reported to affect guard cell K + channels, morphological development and abscisic acid (ABA) responses (Chakravorty et al, 2011). Constitutive expression of AGG3 increases organ size in Arabidopsis (Li et al, 2012), enhances oil production in Camelina sativa (Roy Choudhury et al, 2014) and promotes yield and stress responses in Setaria viridis (Kaur et al, 2018). The phenotype of the Arabidopsis G c triple mutant (agg1agg2agg3) mimics that of agb1, suggesting that all the members of the G protein family have been discovered in Arabidopsis (Thung et al, 2012).…”