Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content

Malachy T. Campbell, Nonoy Bandillo, Fouad Razzaq A. Al Shiblawi, Sandeep Sharma, Kan Liu, Qian Du, Aaron J. Schmitz, Chi Zhang, Anne Aliénor Véry, Aaron J. Lorenz, Harkamal Walia

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

Salinity is a major factor limiting crop productivity. Rice (Oryza sativa), a staple crop for the majority of the world, is highly sensitive to salinity stress. To discover novel sources of genetic variation for salt tolerance-related traits in rice, we screened 390 diverse accessions under 14 days of moderate (9 dS·m-1) salinity. In this study, shoot growth responses to moderate levels of salinity were independent of tissue Na+content. A significant difference in root Na+content was observed between the major subpopulations of rice, with indica accessions displaying higher root Na+and japonica accessions exhibiting lower root Na+content. The genetic basis of the observed variation in phenotypes was elucidated through genome-wide association (GWA). The strongest associations were identified for root Na+:K+ratio and root Na+content in a region spanning ~575 Kb on chromosome 4, named Root Na+Content 4 (RNC4). Two Na+transporters, HKT1;1 and HKT1;4 were identified as candidates for RNC4. Reduced expression of both HKT1;1 and HKT1;4 through RNA interference indicated that HKT1;1 regulates shoot and root Na+content, and is likely the causal gene underlying RNC4. Three non-synonymous mutations within HKT1;1 were present at higher frequency in the indica subpopulation. When expressed in Xenopus oocytes the indica-predominant isoform exhibited higher inward (negative) currents and a less negative voltage threshold of inward rectifying current activation compared to the japonica-predominant isoform. The introduction of a 4.5kb fragment containing the HKT1;1 promoter and CDS from an indica variety into a japonica background, resulted in a phenotype similar to the indica subpopulation, with higher root Na+and Na+:K+. This study provides evidence that HKT1;1 regulates root Na+content, and underlies the divergence in root Na+content between the two major subspecies in rice.

Original languageEnglish (US)
Article numbere1006823
JournalPLoS genetics
Volume13
Issue number6
DOIs
StatePublished - Jan 1 2017

Fingerprint

subspecies
Salinity
Oryza sativa
rice
divergence
Sodium
sodium
Protein Isoforms
Salt-Tolerance
Phenotype
subpopulation
Chromosomes, Human, Pair 4
salinity
Xenopus
RNA Interference
Oocytes
Oryza
phenotype
Genome
Mutation

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content. / Campbell, Malachy T.; Bandillo, Nonoy; Al Shiblawi, Fouad Razzaq A.; Sharma, Sandeep; Liu, Kan; Du, Qian; Schmitz, Aaron J.; Zhang, Chi; Véry, Anne Aliénor; Lorenz, Aaron J.; Walia, Harkamal.

In: PLoS genetics, Vol. 13, No. 6, e1006823, 01.01.2017.

Research output: Contribution to journalArticle

Campbell, MT, Bandillo, N, Al Shiblawi, FRA, Sharma, S, Liu, K, Du, Q, Schmitz, AJ, Zhang, C, Véry, AA, Lorenz, AJ & Walia, H 2017, 'Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content', PLoS genetics, vol. 13, no. 6, e1006823. https://doi.org/10.1371/journal.pgen.1006823
Campbell, Malachy T. ; Bandillo, Nonoy ; Al Shiblawi, Fouad Razzaq A. ; Sharma, Sandeep ; Liu, Kan ; Du, Qian ; Schmitz, Aaron J. ; Zhang, Chi ; Véry, Anne Aliénor ; Lorenz, Aaron J. ; Walia, Harkamal. / Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content. In: PLoS genetics. 2017 ; Vol. 13, No. 6.
@article{f14a797845e144fd9fe3cd79854dcd89,
title = "Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content",
abstract = "Salinity is a major factor limiting crop productivity. Rice (Oryza sativa), a staple crop for the majority of the world, is highly sensitive to salinity stress. To discover novel sources of genetic variation for salt tolerance-related traits in rice, we screened 390 diverse accessions under 14 days of moderate (9 dS·m-1) salinity. In this study, shoot growth responses to moderate levels of salinity were independent of tissue Na+content. A significant difference in root Na+content was observed between the major subpopulations of rice, with indica accessions displaying higher root Na+and japonica accessions exhibiting lower root Na+content. The genetic basis of the observed variation in phenotypes was elucidated through genome-wide association (GWA). The strongest associations were identified for root Na+:K+ratio and root Na+content in a region spanning ~575 Kb on chromosome 4, named Root Na+Content 4 (RNC4). Two Na+transporters, HKT1;1 and HKT1;4 were identified as candidates for RNC4. Reduced expression of both HKT1;1 and HKT1;4 through RNA interference indicated that HKT1;1 regulates shoot and root Na+content, and is likely the causal gene underlying RNC4. Three non-synonymous mutations within HKT1;1 were present at higher frequency in the indica subpopulation. When expressed in Xenopus oocytes the indica-predominant isoform exhibited higher inward (negative) currents and a less negative voltage threshold of inward rectifying current activation compared to the japonica-predominant isoform. The introduction of a 4.5kb fragment containing the HKT1;1 promoter and CDS from an indica variety into a japonica background, resulted in a phenotype similar to the indica subpopulation, with higher root Na+and Na+:K+. This study provides evidence that HKT1;1 regulates root Na+content, and underlies the divergence in root Na+content between the two major subspecies in rice.",
author = "Campbell, {Malachy T.} and Nonoy Bandillo and {Al Shiblawi}, {Fouad Razzaq A.} and Sandeep Sharma and Kan Liu and Qian Du and Schmitz, {Aaron J.} and Chi Zhang and V{\'e}ry, {Anne Ali{\'e}nor} and Lorenz, {Aaron J.} and Harkamal Walia",
year = "2017",
month = "1",
day = "1",
doi = "10.1371/journal.pgen.1006823",
language = "English (US)",
volume = "13",
journal = "PLoS Genetics",
issn = "1553-7390",
publisher = "Public Library of Science",
number = "6",

}

TY - JOUR

T1 - Allelic variants of OsHKT1;1 underlie the divergence between indica and japonica subspecies of rice (Oryza sativa) for root sodium content

AU - Campbell, Malachy T.

AU - Bandillo, Nonoy

AU - Al Shiblawi, Fouad Razzaq A.

AU - Sharma, Sandeep

AU - Liu, Kan

AU - Du, Qian

AU - Schmitz, Aaron J.

AU - Zhang, Chi

AU - Véry, Anne Aliénor

AU - Lorenz, Aaron J.

AU - Walia, Harkamal

PY - 2017/1/1

Y1 - 2017/1/1

N2 - Salinity is a major factor limiting crop productivity. Rice (Oryza sativa), a staple crop for the majority of the world, is highly sensitive to salinity stress. To discover novel sources of genetic variation for salt tolerance-related traits in rice, we screened 390 diverse accessions under 14 days of moderate (9 dS·m-1) salinity. In this study, shoot growth responses to moderate levels of salinity were independent of tissue Na+content. A significant difference in root Na+content was observed between the major subpopulations of rice, with indica accessions displaying higher root Na+and japonica accessions exhibiting lower root Na+content. The genetic basis of the observed variation in phenotypes was elucidated through genome-wide association (GWA). The strongest associations were identified for root Na+:K+ratio and root Na+content in a region spanning ~575 Kb on chromosome 4, named Root Na+Content 4 (RNC4). Two Na+transporters, HKT1;1 and HKT1;4 were identified as candidates for RNC4. Reduced expression of both HKT1;1 and HKT1;4 through RNA interference indicated that HKT1;1 regulates shoot and root Na+content, and is likely the causal gene underlying RNC4. Three non-synonymous mutations within HKT1;1 were present at higher frequency in the indica subpopulation. When expressed in Xenopus oocytes the indica-predominant isoform exhibited higher inward (negative) currents and a less negative voltage threshold of inward rectifying current activation compared to the japonica-predominant isoform. The introduction of a 4.5kb fragment containing the HKT1;1 promoter and CDS from an indica variety into a japonica background, resulted in a phenotype similar to the indica subpopulation, with higher root Na+and Na+:K+. This study provides evidence that HKT1;1 regulates root Na+content, and underlies the divergence in root Na+content between the two major subspecies in rice.

AB - Salinity is a major factor limiting crop productivity. Rice (Oryza sativa), a staple crop for the majority of the world, is highly sensitive to salinity stress. To discover novel sources of genetic variation for salt tolerance-related traits in rice, we screened 390 diverse accessions under 14 days of moderate (9 dS·m-1) salinity. In this study, shoot growth responses to moderate levels of salinity were independent of tissue Na+content. A significant difference in root Na+content was observed between the major subpopulations of rice, with indica accessions displaying higher root Na+and japonica accessions exhibiting lower root Na+content. The genetic basis of the observed variation in phenotypes was elucidated through genome-wide association (GWA). The strongest associations were identified for root Na+:K+ratio and root Na+content in a region spanning ~575 Kb on chromosome 4, named Root Na+Content 4 (RNC4). Two Na+transporters, HKT1;1 and HKT1;4 were identified as candidates for RNC4. Reduced expression of both HKT1;1 and HKT1;4 through RNA interference indicated that HKT1;1 regulates shoot and root Na+content, and is likely the causal gene underlying RNC4. Three non-synonymous mutations within HKT1;1 were present at higher frequency in the indica subpopulation. When expressed in Xenopus oocytes the indica-predominant isoform exhibited higher inward (negative) currents and a less negative voltage threshold of inward rectifying current activation compared to the japonica-predominant isoform. The introduction of a 4.5kb fragment containing the HKT1;1 promoter and CDS from an indica variety into a japonica background, resulted in a phenotype similar to the indica subpopulation, with higher root Na+and Na+:K+. This study provides evidence that HKT1;1 regulates root Na+content, and underlies the divergence in root Na+content between the two major subspecies in rice.

UR - http://www.scopus.com/inward/record.url?scp=85021833956&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85021833956&partnerID=8YFLogxK

U2 - 10.1371/journal.pgen.1006823

DO - 10.1371/journal.pgen.1006823

M3 - Article

VL - 13

JO - PLoS Genetics

JF - PLoS Genetics

SN - 1553-7390

IS - 6

M1 - e1006823

ER -