Distinct roles for SOS1 in the convergent evolution of salt tolerance in eutrema salsugineum and schrenkiella parvula

David E. Jarvis, Choong Hwan Ryu, Mark A Beilstein, Karen S Schumaker

Research output: Contribution to journalArticle

14 Citations (Scopus)

Abstract

Eutrema salsugineum and Schrenkiella parvula are salt-tolerant relatives of the salt-sensitive species Arabidopsis thaliana. An important component of salt tolerance is the regulation of Na+ ion homeostasis, which occurs in part through proteins encoded by the Cation/Proton Antiporter-1 (CPA1) gene family. We used a combination of evolutionary and functional analyses to examine the role of CPA1 genes in the salt tolerance of E. salsugineum and Sc. parvula, and found evidence that changes in CPA1-mediated Na+ extrusion may contribute to the salt tolerance of both species. Specifically, we found that a member of the CPA1 family, the Na+/H+ antiporter gene Salt Overly Sensitive 1 (SOS1), evolved under positive selection in E. salsugineum. In the absence of activation by the SOS2 kinase/SOS3 calcium-binding protein complex, SOS1 from E. salsugineum (EsSOS1) confers greater salt tolerance than SOS1 from Sc. parvula (SpSOS1) and Ar. thaliana (AtSOS1) when expressed in a salt-sensitive strain of Saccharomyces cerevisiae. A single amino acid change in the putative autoinhibitory domain is required but not sufficient for the enhanced salt tolerance conferred by EsSOS1. When activated by SOS2 and SOS3, both EsSOS1 and SpSOS1 confer greater salt tolerance than AtSOS1. Enhanced SOS1-mediated Na+ extrusion therefore appears to contribute to the salt tolerance of both E. salsugineum and Sc. parvula, although through apparently different mechanisms.

Original languageEnglish (US)
Pages (from-to)2094-2107
Number of pages14
JournalMolecular Biology and Evolution
Volume31
Issue number8
DOIs
StatePublished - 2014

Fingerprint

Salt-Tolerance
convergent evolution
salt tolerance
Salts
Antiporters
tolerance
antiporters
salt
salts
Cations
Protons
Arabidopsis
extrusion
Arabidopsis thaliana
cation
Genes
calcium-binding proteins
Sodium-Hydrogen Antiporter
Calcium-Binding Proteins
genes

Keywords

  • convergent evolution
  • CPA1
  • Eutrema salsugineum
  • salt tolerance
  • Schrenkiella parvula
  • SOS1

ASJC Scopus subject areas

  • Genetics
  • Molecular Biology
  • Ecology, Evolution, Behavior and Systematics
  • Medicine(all)

Cite this

Distinct roles for SOS1 in the convergent evolution of salt tolerance in eutrema salsugineum and schrenkiella parvula. / Jarvis, David E.; Ryu, Choong Hwan; Beilstein, Mark A; Schumaker, Karen S.

In: Molecular Biology and Evolution, Vol. 31, No. 8, 2014, p. 2094-2107.

Research output: Contribution to journalArticle

@article{69fa24cf471a465d8f6517421c9c5037,
title = "Distinct roles for SOS1 in the convergent evolution of salt tolerance in eutrema salsugineum and schrenkiella parvula",
abstract = "Eutrema salsugineum and Schrenkiella parvula are salt-tolerant relatives of the salt-sensitive species Arabidopsis thaliana. An important component of salt tolerance is the regulation of Na+ ion homeostasis, which occurs in part through proteins encoded by the Cation/Proton Antiporter-1 (CPA1) gene family. We used a combination of evolutionary and functional analyses to examine the role of CPA1 genes in the salt tolerance of E. salsugineum and Sc. parvula, and found evidence that changes in CPA1-mediated Na+ extrusion may contribute to the salt tolerance of both species. Specifically, we found that a member of the CPA1 family, the Na+/H+ antiporter gene Salt Overly Sensitive 1 (SOS1), evolved under positive selection in E. salsugineum. In the absence of activation by the SOS2 kinase/SOS3 calcium-binding protein complex, SOS1 from E. salsugineum (EsSOS1) confers greater salt tolerance than SOS1 from Sc. parvula (SpSOS1) and Ar. thaliana (AtSOS1) when expressed in a salt-sensitive strain of Saccharomyces cerevisiae. A single amino acid change in the putative autoinhibitory domain is required but not sufficient for the enhanced salt tolerance conferred by EsSOS1. When activated by SOS2 and SOS3, both EsSOS1 and SpSOS1 confer greater salt tolerance than AtSOS1. Enhanced SOS1-mediated Na+ extrusion therefore appears to contribute to the salt tolerance of both E. salsugineum and Sc. parvula, although through apparently different mechanisms.",
keywords = "convergent evolution, CPA1, Eutrema salsugineum, salt tolerance, Schrenkiella parvula, SOS1",
author = "Jarvis, {David E.} and Ryu, {Choong Hwan} and Beilstein, {Mark A} and Schumaker, {Karen S}",
year = "2014",
doi = "10.1093/molbev/msu152",
language = "English (US)",
volume = "31",
pages = "2094--2107",
journal = "Molecular Biology and Evolution",
issn = "0737-4038",
publisher = "Oxford University Press",
number = "8",

}

TY - JOUR

T1 - Distinct roles for SOS1 in the convergent evolution of salt tolerance in eutrema salsugineum and schrenkiella parvula

AU - Jarvis, David E.

AU - Ryu, Choong Hwan

AU - Beilstein, Mark A

AU - Schumaker, Karen S

PY - 2014

Y1 - 2014

N2 - Eutrema salsugineum and Schrenkiella parvula are salt-tolerant relatives of the salt-sensitive species Arabidopsis thaliana. An important component of salt tolerance is the regulation of Na+ ion homeostasis, which occurs in part through proteins encoded by the Cation/Proton Antiporter-1 (CPA1) gene family. We used a combination of evolutionary and functional analyses to examine the role of CPA1 genes in the salt tolerance of E. salsugineum and Sc. parvula, and found evidence that changes in CPA1-mediated Na+ extrusion may contribute to the salt tolerance of both species. Specifically, we found that a member of the CPA1 family, the Na+/H+ antiporter gene Salt Overly Sensitive 1 (SOS1), evolved under positive selection in E. salsugineum. In the absence of activation by the SOS2 kinase/SOS3 calcium-binding protein complex, SOS1 from E. salsugineum (EsSOS1) confers greater salt tolerance than SOS1 from Sc. parvula (SpSOS1) and Ar. thaliana (AtSOS1) when expressed in a salt-sensitive strain of Saccharomyces cerevisiae. A single amino acid change in the putative autoinhibitory domain is required but not sufficient for the enhanced salt tolerance conferred by EsSOS1. When activated by SOS2 and SOS3, both EsSOS1 and SpSOS1 confer greater salt tolerance than AtSOS1. Enhanced SOS1-mediated Na+ extrusion therefore appears to contribute to the salt tolerance of both E. salsugineum and Sc. parvula, although through apparently different mechanisms.

AB - Eutrema salsugineum and Schrenkiella parvula are salt-tolerant relatives of the salt-sensitive species Arabidopsis thaliana. An important component of salt tolerance is the regulation of Na+ ion homeostasis, which occurs in part through proteins encoded by the Cation/Proton Antiporter-1 (CPA1) gene family. We used a combination of evolutionary and functional analyses to examine the role of CPA1 genes in the salt tolerance of E. salsugineum and Sc. parvula, and found evidence that changes in CPA1-mediated Na+ extrusion may contribute to the salt tolerance of both species. Specifically, we found that a member of the CPA1 family, the Na+/H+ antiporter gene Salt Overly Sensitive 1 (SOS1), evolved under positive selection in E. salsugineum. In the absence of activation by the SOS2 kinase/SOS3 calcium-binding protein complex, SOS1 from E. salsugineum (EsSOS1) confers greater salt tolerance than SOS1 from Sc. parvula (SpSOS1) and Ar. thaliana (AtSOS1) when expressed in a salt-sensitive strain of Saccharomyces cerevisiae. A single amino acid change in the putative autoinhibitory domain is required but not sufficient for the enhanced salt tolerance conferred by EsSOS1. When activated by SOS2 and SOS3, both EsSOS1 and SpSOS1 confer greater salt tolerance than AtSOS1. Enhanced SOS1-mediated Na+ extrusion therefore appears to contribute to the salt tolerance of both E. salsugineum and Sc. parvula, although through apparently different mechanisms.

KW - convergent evolution

KW - CPA1

KW - Eutrema salsugineum

KW - salt tolerance

KW - Schrenkiella parvula

KW - SOS1

UR - http://www.scopus.com/inward/record.url?scp=84905041424&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84905041424&partnerID=8YFLogxK

U2 - 10.1093/molbev/msu152

DO - 10.1093/molbev/msu152

M3 - Article

C2 - 24803640

AN - SCOPUS:84905041424

VL - 31

SP - 2094

EP - 2107

JO - Molecular Biology and Evolution

JF - Molecular Biology and Evolution

SN - 0737-4038

IS - 8

ER -