Abstract
Plant growth and grain filling are the key agronomical traits for grain weight and yield of rice. The continuous improvement in rice yield is required for a future sustainable global economy and food security. The heterotrimeric G protein complex containing a canonical α subunit (RGA1) couples extracellular signals perceived by receptors to modulate cell function including plant development and grain weight. We hypothesized that, besides RGA1, three atypical, extra-large GTP-binding protein (XLG) subunits also regulate panicle architecture, plant growth, development, grain weight, and disease resistance. Here, we identified a role of XLGs in agronomic traits and stress tolerance by genetically ablating all three rice XLGs individually and in combination using the CRISPR/Cas9 genome editing in rice. For this study, eight (three single, two double, and three triple) null mutants were selected. Three XLG proteins combinatorically regulate seed filling, because loss confers a decrease in grain weight from 14% with loss of one XLG and loss of three to 32% decrease in grain weight. Null mutations in XLG2 and XLG4 increase grain size. The mutants showed significantly reduced panicle length and number per plant including lesser number of grains per panicle compared to the controls. Loss-of-function of all individual XLGs contributed to 9% more aerial biomass compared to wild type (WT). The double mutant showed improved salinity tolerance. Moreover, loss of the XLG gene family confers hypersensitivity to pathogens. Our findings suggest that the non-canonical XLGs play important roles in regulating rice plant growth, grain filling, panicle phenotype, stress tolerance, and disease resistance. Genetic manipulation of XLGs has the potential to improve agronomic properties in rice.
Highlights
Grain yield has been increased substantially over the past 50 years; a continuous innovation is needed to increase rice production by ∼ 50% from the current level to feed the fastgrowing global population by 2050 (Ray et al, 2013)
Rice (Oryza sativa) seeds of wild-type Nipponbare (WT-NIP) and CRISPR/Cas9-induced Osxlg null mutants were germinated on petri dishes layered with moist filter papers by incubating at 30◦C in the dark for 3 days
Phylogenetic analysis of XLGs from Arabidopsis thaliana, rice, and six other crops revealed two major clades based on the full-length protein sequence, with the clade I and II further divided into three and two subclades, respectively (Figure 1A)
Summary
Grain yield has been increased substantially over the past 50 years; a continuous innovation is needed to increase rice production by ∼ 50% from the current level to feed the fastgrowing global population by 2050 (Ray et al, 2013). Heterotrimeric GTP-binding protein (G protein) complexes regulate numerous cellular functions in higher plant cells (Supplementary Table 1). The canonical plant G protein complex constitutes a guanine nucleotide-binding Gα subunit with GTPase activity, an obligate Gβγ dimer, and a seventransmembrane regulator of G signaling (RGS) protein that modulates activation of Gα (Jones et al, 2011). The activated GTP-bound Gα dissociates from the heterotrimer, and the Gα subunit and the Gβγ dimer target corresponding effectors to initiate the cascades of responses to the external stimuli. In addition to the canonical Gα subunit, plants possess atypical extra-large GTP-binding proteins (XLG) (Assmann, 2002; Jones, 2002; Maruta et al, 2015; Urano et al, 2016). Arabidopsis XLGs interact with AGB1 and AtRGS1 in a nucleotide-independent manner (Lou et al, 2019)
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