Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging

Mining the key genes involved in the balance of rice salt tolerance is extremely important for developing salt-tolerant rice varieties. A library of <i>japonica</i> mutants was screened under salinity conditions to identify putative salt stress-responsive genes. We identified a highly sa...

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Main Authors: Guang Chen, Huimin Han, Xiuli Yang, Ruiying Du, Xu Wang
Format: Article
Language:English
Published: MDPI AG 2022-09-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/23/18/10338
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author Guang Chen
Huimin Han
Xiuli Yang
Ruiying Du
Xu Wang
author_facet Guang Chen
Huimin Han
Xiuli Yang
Ruiying Du
Xu Wang
author_sort Guang Chen
collection DOAJ
description Mining the key genes involved in the balance of rice salt tolerance is extremely important for developing salt-tolerant rice varieties. A library of <i>japonica</i> mutants was screened under salinity conditions to identify putative salt stress-responsive genes. We identified a highly salt-sensitive mutant <i>ss3</i> and used a map-based cloning approach to isolate the gene <i>SS3</i>, which encodes mannose-1-phosphate guanylyltransferase. Under salt treatment, <i>ss3</i> mutants have decreased ascorbic acid (AsA) content and increased reactive oxygen species (ROS) levels compared with the wild type (WT). Exogenous AsA restored the salt tolerance of <i>ss3</i> plants, indicating that inhibition of AsA synthesis was an important factor in the salt sensitivity of the mutant. Functional complementation using the WT allele rescued the mutation, and transcription of <i>SS3</i> was induced by salt stress. Vector <i>SS3p:SS3</i> was constructed containing the 1086 bp coding sequence of <i>SS3</i>. Under salinity conditions, transgenic seedlings expressing <i>SS3p:SS3</i> had improved salt tolerance relative to WT, as demonstrated by better growth status, higher chlorophyll content, a lower level of Na<sup>+</sup>, and a reduced Na<sup>+</sup>/K<sup>+</sup> ratio. Further investigation revealed that several senescence- and autophagy-related genes were expressed at lower levels in salt-stressed transgenic lines compared to WT. These results demonstrate the positive impact of <i>SS3</i> on salt tolerance in rice through the regulation of AsA synthesis and ROS accumulation, and indicate that <i>SS3</i> is a valuable target for genetic manipulation.
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spelling doaj.art-1762f66a3b9b486584b0a1c4a9cdab402023-11-23T16:39:54ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672022-09-0123181033810.3390/ijms231810338Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS ScavengingGuang Chen0Huimin Han1Xiuli Yang2Ruiying Du3Xu Wang4Institute of Quality Standard and Monitoring Technology for Agro-Products of Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaState Key Laboratory of Cotton Biology, Institute of Cotton Research of Chinese Academy of Agricultural Sciences, Anyang 455000, ChinaInstitute of Quality Standard and Monitoring Technology for Agro-Products of Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaInstitute of Quality Standard and Monitoring Technology for Agro-Products of Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaInstitute of Quality Standard and Monitoring Technology for Agro-Products of Guangdong Academy of Agricultural Sciences, Guangzhou 510640, ChinaMining the key genes involved in the balance of rice salt tolerance is extremely important for developing salt-tolerant rice varieties. A library of <i>japonica</i> mutants was screened under salinity conditions to identify putative salt stress-responsive genes. We identified a highly salt-sensitive mutant <i>ss3</i> and used a map-based cloning approach to isolate the gene <i>SS3</i>, which encodes mannose-1-phosphate guanylyltransferase. Under salt treatment, <i>ss3</i> mutants have decreased ascorbic acid (AsA) content and increased reactive oxygen species (ROS) levels compared with the wild type (WT). Exogenous AsA restored the salt tolerance of <i>ss3</i> plants, indicating that inhibition of AsA synthesis was an important factor in the salt sensitivity of the mutant. Functional complementation using the WT allele rescued the mutation, and transcription of <i>SS3</i> was induced by salt stress. Vector <i>SS3p:SS3</i> was constructed containing the 1086 bp coding sequence of <i>SS3</i>. Under salinity conditions, transgenic seedlings expressing <i>SS3p:SS3</i> had improved salt tolerance relative to WT, as demonstrated by better growth status, higher chlorophyll content, a lower level of Na<sup>+</sup>, and a reduced Na<sup>+</sup>/K<sup>+</sup> ratio. Further investigation revealed that several senescence- and autophagy-related genes were expressed at lower levels in salt-stressed transgenic lines compared to WT. These results demonstrate the positive impact of <i>SS3</i> on salt tolerance in rice through the regulation of AsA synthesis and ROS accumulation, and indicate that <i>SS3</i> is a valuable target for genetic manipulation.https://www.mdpi.com/1422-0067/23/18/10338ricesalt stressmannose-1-phosphate guanylyltransferaseascorbic acidreactive oxygen species
spellingShingle Guang Chen
Huimin Han
Xiuli Yang
Ruiying Du
Xu Wang
Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
International Journal of Molecular Sciences
rice
salt stress
mannose-1-phosphate guanylyltransferase
ascorbic acid
reactive oxygen species
title Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
title_full Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
title_fullStr Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
title_full_unstemmed Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
title_short Salt Tolerance of Rice Is Enhanced by the <i>SS3</i> Gene, Which Regulates Ascorbic Acid Synthesis and ROS Scavenging
title_sort salt tolerance of rice is enhanced by the i ss3 i gene which regulates ascorbic acid synthesis and ros scavenging
topic rice
salt stress
mannose-1-phosphate guanylyltransferase
ascorbic acid
reactive oxygen species
url https://www.mdpi.com/1422-0067/23/18/10338
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AT xiuliyang salttoleranceofriceisenhancedbytheiss3igenewhichregulatesascorbicacidsynthesisandrosscavenging
AT ruiyingdu salttoleranceofriceisenhancedbytheiss3igenewhichregulatesascorbicacidsynthesisandrosscavenging
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