Heterotrimeric G-protein α subunit (RGA1) regulates tiller development, yield, cell wall, nitrogen response and biotic stress in rice

Pathak, Rashmi; Mandal, Vikas Kumar; Jangam, Annie Prasanna; Sharma, Nikhil; Madan, Bhumika; Jaiswal, Dinesh Kumar; Raghuram, Nandula

doi:10.1038/s41598-021-81824-1

Cited by 17 publications

(13 citation statements)

References 88 publications

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“…This is evidenced by genome sequences of 3000 rice genotypes ( Li et al, 2014 ) and growing functional genomics of N ( Li et al, 2018 ; Pathak et al, 2020 ; Mandal et al, 2022 ). Further, the recent NUE phenotype ( Sharma et al, 2018 , 2021 ; Pathak et al, 2021 ) growing quantitative trait loci (QTL) and genotyping ( Kumari et al, 2021 ) make rice an ideal target crop for NUE improvement. A recent simulation showed that $743 million per year could be saved by a 20% increase in rice NUE ( Langholtz et al, 2021 ), while the global expenditure in that direction is not even a tiny fraction of it.…”

Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomic Analyses of Nitrate-Response in Rice Genotypes With Contrasting Nitrogen Use Efficiency Reveals Common and Genotype-Specific Processes, Molecular Targets and Nitrogen Use Efficiency-Candidates

et al. 2022

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The genetic basis for nitrogen (N)-response and N use efficiency (NUE) must be found in N-responsive gene expression or protein regulation. Our transcriptomic analysis of nitrate response in two contrasting rice genotypes of Oryza sativa ssp. Indica (Nidhi with low NUE and Panvel1 with high NUE) revealed the processes/functions underlying differential N-response/NUE. The microarray analysis of low nitrate response (1.5 mM) relative to normal nitrate control (15 mM) used potted 21-days old whole plants. It revealed 1,327 differentially expressed genes (DEGs) exclusive to Nidhi and 666 exclusive to Panvel1, apart from 70 common DEGs, of which 10 were either oppositely expressed or regulated to different extents. Gene ontology analyses revealed that photosynthetic processes were among the very few processes common to both the genotypes in low N response. Those unique to Nidhi include cell division, nitrogen utilization, cytoskeleton, etc. in low N-response, whereas those unique to Panvel1 include signal transduction, protein import into the nucleus, and mitochondria. This trend of a few common but mostly unique categories was also true for transporters, transcription factors, microRNAs, and post-translational modifications, indicating their differential involvement in Nidhi and Panvel1. Protein-protein interaction networks constructed using DEG-associated experimentally validated interactors revealed subnetworks involved in cytoskeleton organization, cell wall, etc. in Nidhi, whereas in Panvel1, it was chloroplast development. NUE genes were identified by selecting yield-related genes from N-responsive DEGs and their co-localization on NUE-QTLs revealed the differential distribution of NUE-genes between genotypes but on the same chromosomes 1 and 3. Such hotspots are important for NUE breeders.

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Section: Introductionmentioning

confidence: 99%

Comparative Transcriptomic Analyses of Nitrate-Response in Rice Genotypes With Contrasting Nitrogen Use Efficiency Reveals Common and Genotype-Specific Processes, Molecular Targets and Nitrogen Use Efficiency-Candidates

et al. 2022

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“…Some studies have demonstrated that G protein plays a vital role in regulating low-nitrogen stress in plants (Sun et al, 2014; Liang et al, 2018; Kaur et al, 2018; Pathak et al, 2021). However, the potential regulatory mechanism remains largely unknown.…”

Section: Discussionmentioning

confidence: 99%

“…In general, following receptor-mediated activation, the heterotrimeric G protein transmits external signals to cells via various downstream cytosolic effectors to regulate biological processes (Bommert et al, 2013; Urano et al, 2015; Lee et al, 2017; Roy et al, 2019). AtGPA1 phosphorylates ABA-insensitive 1 ( ABI1 ) and phospholipase Dα1 ( PLDα1 ) to regulate ABA-dependent stomatal opening and closure in Arabidopsis (Roy et al, 2016; Hei et al, 2018; Pathak et al, 2021). The heterotrimeric G protein also interacts with plant-specific receptor-like kinases (RLKs) and receptor-like proteins (RLPs) to regulate multiple immune responses, shoot apical meristem development, and nodule formation (Bommert et al, 2013; Aranda et al, 2015; Pandey, 2020).…”

Section: Discussionmentioning

confidence: 99%

“…In Arabidopsis , heterotrimeric G proteins consist of one canonical α subunit (GPA1), one β subunit (AGB1), and at least three γ subunits (AGG), all of which play crucial roles in almost all aspects of growth and development (Pathak et al, 2021). During biotic and abiotic stress, these proteins also control key agronomic traits, including crop yield (Pandey, 2019).…”

Section: Introductionmentioning

confidence: 99%

“…Further evidence has indicated that DEP1 can interact with other two G protein subunits, RGA1 (G protein α subunit) and RGB1 (G protein β subunit), to regulate NUE and yield in rice (Huang et al, 2014). Increasing evidence has revealed that RGA1 also regulates the nitrogen-signaling pathway through other genes, such the bHLH gene family members, nitrite reductase, OsCIPK23 , and urea transporters in rice (Pathak et al, 2021). Setaria plants overexpressing AGG3 (rice homologs of the Arabidopsis group III Gγ subunit) exhibit better growth during early development under conditions of low nitrogen (Kaur et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

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Heterotrimeric G protein α subunit (GPA1) regulates the response to low-nitrogen stress in Arabidopsis by interacting with AtNRT1.4 and AtATG8a

Luo

et al. 2022

Preprint

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Efficient nitrogen absorption and utilization are important factors for higher plants to increase yield and reduce eutrophication (caused by excessive use of nitrogen fertilizers). Heterotrimeric G proteins participate in the pathway regulating nitrogen absorption and utilization in plants. However, the regulatory mechanism remains largely obscured. In this study, our results revealed that mutant gpa1-4 was tolerant to low-nitrogen stress in Arabidopsis. AtGPA1 was shown to directly interact with a nitrate transporter (AtNRT1.4) and a key autophagy-related protein (AtATG8a) on the plasma membrane. GUS staining and subcellular localization showed that AtGPA1 and AtNRT1.4 were co-expressed in roots and leaf veins and on the plasma membrane. Under low-nitrate conditions, the single mutant gpa1-4 and NRT1.4RNAi plants (AtNRT1.4RNA interference plants) and the double mutant NRT1.4RNAi/gpa1-4 plants (AtNRT1.4RNA interference plants on a gpa1-4 background) were healthier than the wild type plants. Moreover, the phenotype of the double mutant NRT1.4RNAi/gpa1-4 plants was closer to that of the NRT1.4RNAi plants compared to that of the gpa1-4 mutants. The results of the nitrate efflux rate assay in roots were consistent with the phenotypic changes under low-nitrogen conditions. These results indicated that AtGPA1 is an upstream factor that regulated the response to low-nitrogen stress through interaction with AtNRT1.4. In addition, we found that transgenic plants overexpressing AtATG8a were more tolerant to low-nitrogen stress, and their phenotype was similar to that of gpa1-4 mutants and double mutant ATG8aOX/gpa1-4 plants. Our findings may provide a new model for improving nitrogen-use efficiency through genetical modification to boost crop yields.

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Nitrate-responsive transcriptome analysis of rice RGA1 mutant reveals the role of G-protein alpha subunit in negative regulation of nitrogen-sensitivity and use efficiency

Prasanna,

Mandal,

Kumar

et al. 2023

Plant Cell Rep

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Nitrogen (N) use e ciency (NUE) is important for sustainable agriculture. G-protein signalling was implicated in N-response/NUE in rice, but needs genetic characterization of the role of α subunit (RGA1). We found that RGA1 knock-out mutant in japonica rice exhibited lesser nitrate-dose sensitivity, higher yield and NUE relative to the wild type (WT). We investigated its genomewide basis using nitrateresponsive rga1 transcriptome relative to WT. It revealed 3,416 differentially expressed genes (DEGs), including 719 associated with development, grain yield and phenotypic traits for NUE. The upregulated DEGs were related to photosynthesis, chlorophyll, tetrapyrrole and porphyrin biosynthesis, while the downregulated DEGs belonged to cellular protein metabolism and transport, small GTPase signalling, cell redox homeostasis etc. RT-qPCR validated 26 nitrate-responsive DEGs across functional categories. Physiological validation of nitrate-response in the mutant and WT at 1.5 and 15 mM doses revealed higher chlorophyll and stomatal length but decreased stomatal density, conductance and transpiration.The consequent increase in photosynthesis and water use e ciency may contribute to higher yield and NUE in the mutant, whereas the WT was N-dose sensitive. The mutant was not as N dose-responsive as WT in shoot/root growth, productive tillers and heading date, but equally responsive as WT in total N and protein content. RGA1mutant is less impacted by higher N-dose or salt stress in terms of yield, protein content, photosynthetic performance, relative water content, water use e ciency and catalase activity. PPI-network analyses revealed known NUE-related proteins as RGA1 interactors. Therefore, RGA1 regulates N-dose sensitivity and NUE in rice. Key MessageNitrate-responsive transcriptomic, phenotypic and physiological analyses of rice RGA1 mutant revealed many novel RGA1-regulated genes/processes/traits related to nitrogen use e ciency, and provided robust genetic evidence of RGA1-regulation of NUE.

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Heterotrimeric G-protein α subunit (RGA1) regulates tiller development, yield, cell wall, nitrogen response and biotic stress in rice

Cited by 17 publications

References 88 publications

Comparative Transcriptomic Analyses of Nitrate-Response in Rice Genotypes With Contrasting Nitrogen Use Efficiency Reveals Common and Genotype-Specific Processes, Molecular Targets and Nitrogen Use Efficiency-Candidates

Comparative Transcriptomic Analyses of Nitrate-Response in Rice Genotypes With Contrasting Nitrogen Use Efficiency Reveals Common and Genotype-Specific Processes, Molecular Targets and Nitrogen Use Efficiency-Candidates

Heterotrimeric G protein α subunit (GPA1) regulates the response to low-nitrogen stress in Arabidopsis by interacting with AtNRT1.4 and AtATG8a

Nitrate-responsive transcriptome analysis of rice RGA1 mutant reveals the role of G-protein alpha subunit in negative regulation of nitrogen-sensitivity and use efficiency

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