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.2018 Jan 5:8:2216.
doi: 10.3389/fpls.2017.02216. eCollection 2017.

Variation in the Abundance ofOsHAK1 Transcript Underlies the Differential Salinity Tolerance of anindica and ajaponica Rice Cultivar

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Variation in the Abundance ofOsHAK1 Transcript Underlies the Differential Salinity Tolerance of anindica and ajaponica Rice Cultivar

Guang Chen et al. Front Plant Sci..

Abstract

Salinity imposes a major constraint over the productivity of rice. A set of chromosome segment substitution lines (CSSLs), derived from a cross between thejaponica type cultivar (cv.) Nipponbare (salinity sensitive) and theindica type cv. 9311 (moderately tolerant), was scored using a hydroponics system for their salinity tolerance at the seedling stage. Two of the CSSLs, which share a ∼1.2 Mbp stretch of chromosome 4 derived from cv. Nipponbare, were as sensitive to the stress as cv. Nipponbare itself. Fine mapping based on an F2 population bred from a backcross between one of these CSSLs and cv. 9311 narrowed this region to 95 Kbp, within which only one gene (OsHAK1) exhibited a differential (lower) transcript abundance in cv. Nipponbare and the two CSSLs compared to in cv. 9311. The gene was up-regulated by exposure to salinity stress both in the root and the shoot, while a knockout mutant proved to be more salinity sensitive than its wild type with respect to its growth at both the vegetative and reproductive stages. Seedlings over-expressingOsHAK1 were more tolerant than wild type, displaying a superior photosynthetic rate, a higher leaf chlorophyll content, an enhanced accumulation of proline and a reduced level of lipid peroxidation. At the transcriptome level, the over-expression ofOsHAK1 stimulated a number of stress-responsive genes as well as four genes known to be involved in Na+ homeostasis and the salinity response (OsHKT1;5,OsSOS1,OsLti6a andOsLti6b). When the stress was applied at booting through to maturity, theOsHAK1 over-expressors out-yielded wild type by 25%, and no negative pleiotropic effects were expressed in plants gown under non-saline conditions. The level of expression ofOsHAK1 was correlated with Na+/K+ homeostasis, which implies that the gene should be explored a target for molecular approaches to the improvement of salinity tolerance in rice.

Keywords: 9311; Na+ and K+ homeostasis; Nipponbare; Oryza sativa; OsHAK1; salinity stress.

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Figures

FIGURE 1
FIGURE 1
The contrasting salinity tolerance of the rice cvs Nipponbare and 9311, and two derived CSSLs. Seedlings were exposed to 100 mM NaCl for 7 days.(A,B) The growth and appearance of the plants raised in(A) the absence of NaCl,(B) the presence of 100 mM NaCl. White bars: 5 cm, yellow bars: 1 cm.(C) Dry matter accumulation,(D) [K+],(E) [K+]/[Na+] ratio and(F) the abundance ofOsHAK1 transcript. Values shown in the form of mean ± SE (n = 5). Means labeled with the same lower case letter did not differ significantly from one another (P < 0.05).
FIGURE 2
FIGURE 2
Graphical genotypes uncovered in the critical region of chromosome 4 among F2 progeny derived from the cross CSSL-1 x cv. 9311. The unfilled regions represent those homozygous for cv. 9311 alleles, and the filled ones represent those homozygous for cv. Nipponbare alleles. Mean shoot biomass values ± SE (n = 5) are shown on the right.∗Mean differs significantly (P < 0.05) between cv. 9311 and genotypes carrying the critical chromosome 4 segment inherited from cv. Nipponbare.
FIGURE 3
FIGURE 3
The effect of salinity stress (100 mM NaCl for 0–24 h) on the transcription ofOsHAK1 in(A) the roots and(B) the shoots of WT seedlings. Transcript abundances were derived using qRT-PCR, withUbq chosen as the reference sequence. The abundance ofOsHAK1 transcript prior to the salinity treatment was set arbitrarily as 1. The whiskers indicate the SE (n = 3).
FIGURE 4
FIGURE 4
Complementation of a salinity-sensitive yeast mutant byOsHAK1.(A) Yeast cells harboring an empty vector (pYES2) are shown in the upper row, and those harboringOsHAK1 in the lower row. The(B) [K+] and(C) [Na+] of yeast cells grown either in the absence (control) or presence of 50 mM NaCl. Data represent the mean ± SE (n = 3). Significant differences (P < 0.05) between the performance of cells harboring the empty vector and those harboring theOsHAK1 transgene are indicated by an asterisk. ns, non-significant difference; DW, dry weight.
FIGURE 5
FIGURE 5
The effect ofOsHAK1 on the growth of rice seedlings.(A) The growth of anOsHAK1 over-expressor (Ox1) and WT in either non-salinized (control) or salinized (100 mM NaCl) medium.(B) The growth of anOsHAK1 knock-out mutant (oshak1-M) and its WT in either non-salinized (control) or salinized (100 mM NaCl) medium. Bar: 10 cm.(C,D) Dry matter accumulation of seedings raised in either non-salinized (control) or salinized (100 mM NaCl) medium:(C) the root and(D) the shoot. Values shown in the form mean ± SE (n = 5). Significant differences (P < 0.05) between the test genotype and WT are indicated by an asterisk. ns, non-significant difference; WT-D, cv. Dongjin; WT-N, cv. Nipponbare; WT-M, cv. Manan,oshak1-D, oshak1-M:OsHAK1 knockout mutants in, respectively a cv. Dongjin and a cv. Manan background.
FIGURE 6
FIGURE 6
The effect ofOsHAK1 on Na+ accumulation and the [Na+]/[K+] ratio in seedlings challenged by salinity stress. [Na+] in(A) the root and(B) the shoot. The [Na+]/[K+] ratio in(C) the root and(D) the shoot. Values shown in the form mean ± SE (n = 5). Significant differences (P < 0.05) between the test genotype and WT are indicated by an asterisk. ns, non-significant difference. DW, dry weight.
FIGURE 7
FIGURE 7
The abundance of transcript from genes encoding Na+ transporters.(A–D) The transcription in the roots of hydroponically-grown seedlings raised either in the presence or absence of salinity stress:(A)OsHKT1;5,(B)OsSOS1,(C)OsLti6a,(D)OsLti6b. Outputs derived from qRT-PCRs were normalized against the abundance ofUbq transcript. Values shown in the form mean ± SE (n = 3). Significant differences (P < 0.05) between the test genotype and WT are indicated by an asterisk. ns, non-significant difference.
FIGURE 8
FIGURE 8
The effect ofOsHAK1 on the physiology of soil-grown plants exposed to salinity stress.(A) Photosynthetic rate,(B) leaf chlorophyll content,(C) H2O2 content,(D) relative electrolyte leakage,(E) MDA content and(F) proline content. Values shown in the form mean ± SE (n = 5). Significant differences (P < 0.05) between the test genotype and WT are indicated by an asterisk. ns, non-significant; FW, fresh weight.
FIGURE 9
FIGURE 9
The effect ofOsHAK1 on the transcription of selected stress-responsive genes.(A–D) The transcription in the youngest two leaves of soil-grown plants in the presence or absence of salinity stress:(A)OsP5CS1,(B)OsDREB2A,(C)OsAP37,(D)OsERD1. Outputs derived from qRT-PCRs were normalized against the abundance ofUbq transcript. Values shown in the form mean ± SE (n = 3). Significant differences (P < 0.05) between the test genotype and WT are indicated by an asterisk. ns, non-significant difference.
FIGURE 10
FIGURE 10
The over-expression ofOsHAK1 raises the level of rice’s salinity tolerance at the reproductive stage. The stress was applied at the booting stage and maintained through to maturity.(A) Effective tiller number per plant,(B) seed set,(C) 1000 grain weight and(D) grain yield per plant. Values shown in the form mean ± SE (n = 5). Significant differences (P < 0.05) between the over-expressor and WT are indicated by an asterisk. ns, non-significant difference.
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