Heterotrimeric G proteins are important transducers of receptor signaling, functioning in plants with CLAVATA receptors in controlling shoot meristem size and with pathogen-associated molecular pattern receptors in basal immunity. However, whether specific members of the heterotrimeric complex potentiate cross-talk between development and defense, and the extent to which these functions are conserved across species, have not yet been addressed. Here we used CRISPR/Cas9 to knock out the maize G protein β subunit gene (Gβ) and found that the mutants are lethal, differing from those in Arabidopsis, in which homologous mutants have normal growth and fertility. We show that lethality is caused not by a specific developmental arrest, but by autoimmunity. We used a genetic diversity screen to suppress the lethal Gβ phenotype and also identified a maize Gβ allele with weak autoimmune responses but strong development phenotypes. Using these tools, we show that Gβ controls meristem size in maize, acting epistatically with G protein α subunit gene (Gα), suggesting that Gβ and Gα function in a common signaling complex. Furthermore, we used an association study to show that natural variation in Gβ influences maize kernel row number, an important agronomic trait. Our results demonstrate the dual role of Gβ in immunity and development in a cereal crop and suggest that it functions in cross-talk between these competing signaling networks. Therefore, modification of Gβ has the potential to optimize the trade-off between growth and defense signaling to improve agronomic production.

The maize heterotrimeric G protein β subunit controls shoot meristem development and immune responses

Heterotrimeric GTP binding proteins (G proteins) and cytokinin play important roles in regulating plant growth and development. However, little is known about the mechanism by which they coordinate the regulation of grain size in rice. We functionally characterized one gene, RGG1, encoding a type-A Gγ subunit. Strong GUS staining was detected in young panicles and spikelets, suggesting a role for this gene in modulating panicle-related trait development. Overexpression of RGG1 in Nipponbare (NIP) and Wuyunjing 30 (WYJ30) significantly decreased plant height, panicle length and grain length by regulating cell division. However, rgg1 mutants generated by the CRISPR/Cas9 system exhibited no obvious phenotypic differences, which may be due to the extremely low expression level of this gene in vivo. The transcriptomes of young panicles of NIP, the NIP-rgg1–2 mutant and the NIP-OE2 overexpression line were sequenced, and the results showed that many differentially expressed genes (DEGs) were associated with the cytokinin biosynthetic pathway. We confirmed this result by measuring the endogenous cytokinin levels and found that cytokinin content was lower in the overexpression lines. Additionally, increased expression of RGG1 decreased sensitivity to low concentrations of 6-benzylaminopurine (6-BA). Our results reveal a novel G protein—cytokinin module controlling grain size in rice and will be beneficial for understanding the mechanisms by which G proteins regulate grain size and plant development.

/pdf/rgg1-involved-in-the-cytokinin-regulatory-pathway-controls-2gmipxno0w.pdf

RGG1, Involved in the Cytokinin Regulatory Pathway, Controls Grain Size in Rice

Nutrient stresses induce foliar chlorosis and growth defects. Here we propose heterotrimeric G proteins as signaling mediators of various nutrient stresses, through meta-analyses of >20 transcriptomic data sets associated with nutrient stresses or G protein mutations. Systematic comparison of transcriptomic data yielded 104 genes regulated by G protein subunits under common nutrient stresses: 69 genes under Gβ subunit (AGB1) control and 35 genes under Gα subunit (GPA1) control. Quantitative real-time PCR experiments validate that several transcription factors and metal transporters changed in expression level under suboptimal iron, zinc, and/or copper concentrations, while being misregulated in the Arabidopsis Gβ-null (agb1) mutant. The agb1 mutant had altered metal ion profiles and exhibited severe growth arrest under zinc stress, and aberrant root waving under iron and zinc stresses, while the Gα-null mutation attenuated leaf chlorosis under iron deficiency in both Arabidopsis and rice. Our transcriptional network analysis inferred computationally that WRKY-family transcription factors mediate the AGB1-dependent nutrient responses. As corroborating evidence of our inference, ectopic expression of WRKY25 or WRKY33 rescued the zinc stress phenotypes and the expression of zinc transporters in the agb1-2 background. These results, together with Gene Ontology analyses, suggest two contrasting roles for G protein-coupled signaling pathways in micronutrient stress responses: one enhancing general stress tolerance and the other modulating ion homeostasis through WRKY transcriptional regulatory networks. In addition, tolerance to iron stress in the rice Gα mutant provides an inroad to improve nutrient stress tolerance of agricultural crops by manipulating G protein signaling.

Crosstalk between heterotrimeric G protein-coupled signaling pathways and WRKY transcription factors modulating plant responses to suboptimal micronutrient conditions.

Heterotrimeric G-proteins are complexes that regulate important signalling pathways essential for growth and development in both plants and animals. Although plant cells are composed of the core components (Gα, Gβ and Gγ subunits) found in animal G-proteins, the complexities of the architecture, function and signalling mechanisms of those in animals are dissimilar to those identified in some plants. Current studies on plant G-proteins have improved knowledge of the essential physiological and agronomic properties, which when harnessed, could potentially impact global food security. Extensive studies on the molecular mechanisms underlying these properties in diverse plant species will be imperative in improving our current understanding of G-protein signalling pathways involved in plant growth and development. The advancement of G-protein signalling networks in distinct plant species could significantly aid in better crop development. This review summarizes current progress, novel discoveries and future prospects for this area in potential crop improvement.

Signal transduction by plant heterotrimeric G-protein.

• Low light intensities affect the outbreak of plant diseases. However, the underlying molecular mechanisms remain poorly understood. • HPLC analysis of tomato (Solanum lycopersicum) revealed that apoplastic glucose (Glc) levels decreased in response to low light. Conversely, low light-induced susceptibility to Pseudomonas syringae pv. tomato (Pst) DC3000 was significantly alleviated by exogenous Glc treatment. Using cell-based biolayer interferometry assays, we found that Glc specifically binds to the tomato regulator of G protein signaling 1 (RGS1). Laser scanning confocal microscopy imaging revealed that Glc triggers RGS1 endocytosis, which influences the uncoupling of the RGS1-Gα (GPA1) and GPA1-Gβ (SlGB1) proteins, in a dose- and duration-dependent manner. • Analysis of G protein single and double mutants revealed that RGS1 negatively regulates disease resistance under low light and is required for Glc-enhanced defense. Downstream of RGS1-Glc binding, GPA1 negatively mediates the light intensity-regulated defense, while SlGB1 positively regulates this process. • These results reveal a novel light intensity-responsive defense system that is mediated by a Glc-RGS1-G protein signaling pathway. This information will be critical for future investigations of how plant cells sense extracellular sugars and adjust defense under different environments, as well as genetic engineering approaches to improve stress resilience.

Glucose sensing by regulator of G protein signaling 1 (RGS1) plays a crucial role in coordinating defense in response to environmental variation in tomato.

The heterotrimeric G protein β subunit RGB1 plays an important role in plant growth and development. However, the molecular mechanisms underlying the regulation of rice growth by RGB1 remain elusive. Here, the rgb1 mutants rgb1–1 (+ 1 bp), rgb1–2 (− 1 bp), and rgb1–3 (− 11 bp) were isolated using the CRISPR/Cas9 system, and they were arrested at 1 day after germination and ultimately exhibited seedling lethality. The dynamic anatomical characteristics of the embryos of the rgb1 seedlings and WT during early postgermination and according to TUNEL assays showed that the suppressed growth of the rgb1 mutants was caused by cell death. In addition to the limited shoot and root development, the development of the embryo shoot-root axis was suppressed in the rgb1 mutants. RGB1 was expressed mainly in the root epidermal and vascular tissues of the embryo. Moreover, transcript profiling analysis revealed that the expression of a large number of auxin-, cytokinin-, and brassinosteroid-inducible genes was upregulated or downregulated in the rgb1 mutant compared to the wild type during seedling development. Overall, the rgb1 mutants provide an ideal material for exploring the molecular mechanism underlying rice seedling formation during early postgermination development by G proteins. The heterotrimeric G protein β subunit RGB1 acts as a crucial factor in promoting early postgermination seedling development in rice.

/pdf/the-heterotrimeric-g-protein-b-subunit-rgb1-is-required-for-2pprk6tmbl.pdf

The heterotrimeric G protein β subunit RGB1 is required for seedling formation in rice.

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The heterotrimeric G protein β subunit RGB1 is required for seedling formation in rice.