A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses

Sugarcane (Saccharum spp.) is a prominent source of sugar and serves as bioenergy/biomass feedstock globally. Multiple biotic and abiotic stresses, including drought, salinity, and cold, adversely affect sugarcane yield. G-protein-coupled receptors (GPCRs) are components of G-protein-mediated signal...

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Autores principales:	Manikandan Ramasamy, Mona B. Damaj, Carol Vargas-Bautista, Victoria Mora, Jiaxing Liu, Carmen S. Padilla, Sonia Irigoyen, Tripti Saini, Nirakar Sahoo, Jorge A. DaSilva, Kranthi K. Mandadi
Formato:	article
Lenguaje:	EN
Publicado:	Frontiers Media S.A. 2021
Materias:	abiotic stresses G-protein-coupled receptor sugarcane transgenics bioenergy and biofuel Plant culture SB1-1110
Acceso en línea:	https://doaj.org/article/0234c3ade7dc4c909014dd8b7e452ec1
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spelling	oai:doaj.org-article:0234c3ade7dc4c909014dd8b7e452ec12021-11-11T10:16:47ZA Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses1664-462X10.3389/fpls.2021.745891https://doaj.org/article/0234c3ade7dc4c909014dd8b7e452ec12021-11-01T00:00:00Zhttps://www.frontiersin.org/articles/10.3389/fpls.2021.745891/fullhttps://doaj.org/toc/1664-462XSugarcane (Saccharum spp.) is a prominent source of sugar and serves as bioenergy/biomass feedstock globally. Multiple biotic and abiotic stresses, including drought, salinity, and cold, adversely affect sugarcane yield. G-protein-coupled receptors (GPCRs) are components of G-protein-mediated signaling affecting plant growth, development, and stress responses. Here, we identified a GPCR-like protein (ShGPCR1) from sugarcane and energy cane (Saccharum spp. hybrids) and characterized its function in conferring tolerance to multiple abiotic stresses. ShGPCR1 protein sequence contained nine predicted transmembrane (TM) domains connected by four extracellular and four intracellular loops, which could interact with various ligands and heterotrimeric G proteins in the cells. ShGPCR1 sequence displayed other signature features of a GPCR, such as a putative guanidine triphosphate (GTP)-binding domain, as well as multiple myristoylation and protein phosphorylation sites, presumably important for its biochemical function. Expression of ShGPCR1 was upregulated by drought, salinity, and cold stresses. Subcellular imaging and calcium (Ca2+) measurements revealed that ShGPCR1 predominantly localized to the plasma membrane and enhanced intracellular Ca2+ levels in response to GTP, respectively. Furthermore, constitutive overexpression of ShGPCR1 in sugarcane conferred tolerance to the three stressors. The stress-tolerance phenotype of the transgenic lines corresponded with activation of multiple drought-, salinity-, and cold-stress marker genes, such as Saccharum spp. LATE EMBRYOGENESIS ABUNDANT, DEHYDRIN, DROUGHT RESPONSIVE 4, GALACTINOL SYNTHASE, ETHYLENE RESPONSIVE FACTOR 3, SALT OVERLY SENSITIVE 1, VACUOLAR Na+/H+ ANTIPORTER 1, NAM/ATAF1/2/CUC2, COLD RESPONSIVE FACTOR 2, and ALCOHOL DEHYDROGENASE 3. We suggest that ShGPCR1 plays a key role in conferring tolerance to multiple abiotic stresses, and the engineered lines may be useful to enhance sugarcane production in marginal environments with fewer resources.Manikandan RamasamyMona B. DamajCarol Vargas-BautistaVictoria MoraJiaxing LiuCarmen S. PadillaSonia IrigoyenTripti SainiNirakar SahooJorge A. DaSilvaJorge A. DaSilvaKranthi K. MandadiKranthi K. MandadiFrontiers Media S.A.articleabiotic stressesG-protein-coupled receptorsugarcanetransgenicsbioenergy and biofuelPlant cultureSB1-1110ENFrontiers in Plant Science, Vol 12 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	abiotic stresses G-protein-coupled receptor sugarcane transgenics bioenergy and biofuel Plant culture SB1-1110
spellingShingle	abiotic stresses G-protein-coupled receptor sugarcane transgenics bioenergy and biofuel Plant culture SB1-1110 Manikandan Ramasamy Mona B. Damaj Carol Vargas-Bautista Victoria Mora Jiaxing Liu Carmen S. Padilla Sonia Irigoyen Tripti Saini Nirakar Sahoo Jorge A. DaSilva Jorge A. DaSilva Kranthi K. Mandadi Kranthi K. Mandadi A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
description	Sugarcane (Saccharum spp.) is a prominent source of sugar and serves as bioenergy/biomass feedstock globally. Multiple biotic and abiotic stresses, including drought, salinity, and cold, adversely affect sugarcane yield. G-protein-coupled receptors (GPCRs) are components of G-protein-mediated signaling affecting plant growth, development, and stress responses. Here, we identified a GPCR-like protein (ShGPCR1) from sugarcane and energy cane (Saccharum spp. hybrids) and characterized its function in conferring tolerance to multiple abiotic stresses. ShGPCR1 protein sequence contained nine predicted transmembrane (TM) domains connected by four extracellular and four intracellular loops, which could interact with various ligands and heterotrimeric G proteins in the cells. ShGPCR1 sequence displayed other signature features of a GPCR, such as a putative guanidine triphosphate (GTP)-binding domain, as well as multiple myristoylation and protein phosphorylation sites, presumably important for its biochemical function. Expression of ShGPCR1 was upregulated by drought, salinity, and cold stresses. Subcellular imaging and calcium (Ca2+) measurements revealed that ShGPCR1 predominantly localized to the plasma membrane and enhanced intracellular Ca2+ levels in response to GTP, respectively. Furthermore, constitutive overexpression of ShGPCR1 in sugarcane conferred tolerance to the three stressors. The stress-tolerance phenotype of the transgenic lines corresponded with activation of multiple drought-, salinity-, and cold-stress marker genes, such as Saccharum spp. LATE EMBRYOGENESIS ABUNDANT, DEHYDRIN, DROUGHT RESPONSIVE 4, GALACTINOL SYNTHASE, ETHYLENE RESPONSIVE FACTOR 3, SALT OVERLY SENSITIVE 1, VACUOLAR Na+/H+ ANTIPORTER 1, NAM/ATAF1/2/CUC2, COLD RESPONSIVE FACTOR 2, and ALCOHOL DEHYDROGENASE 3. We suggest that ShGPCR1 plays a key role in conferring tolerance to multiple abiotic stresses, and the engineered lines may be useful to enhance sugarcane production in marginal environments with fewer resources.
format	article
author	Manikandan Ramasamy Mona B. Damaj Carol Vargas-Bautista Victoria Mora Jiaxing Liu Carmen S. Padilla Sonia Irigoyen Tripti Saini Nirakar Sahoo Jorge A. DaSilva Jorge A. DaSilva Kranthi K. Mandadi Kranthi K. Mandadi
author_facet	Manikandan Ramasamy Mona B. Damaj Carol Vargas-Bautista Victoria Mora Jiaxing Liu Carmen S. Padilla Sonia Irigoyen Tripti Saini Nirakar Sahoo Jorge A. DaSilva Jorge A. DaSilva Kranthi K. Mandadi Kranthi K. Mandadi
author_sort	Manikandan Ramasamy
title	A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
title_short	A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
title_full	A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
title_fullStr	A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
title_full_unstemmed	A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses
title_sort	sugarcane g-protein-coupled receptor, shgpcr1, confers tolerance to multiple abiotic stresses
publisher	Frontiers Media S.A.
publishDate	2021
url	https://doaj.org/article/0234c3ade7dc4c909014dd8b7e452ec1
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A Sugarcane G-Protein-Coupled Receptor, ShGPCR1, Confers Tolerance to Multiple Abiotic Stresses

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