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Sl HAK 20: a new player in plant salt tolerance

2020; Springer Nature; Volume: 39; Issue: 10 Linguagem: Inglês

10.15252/embj.2020104997

1460-2075

Yanli Xiang, José M. Jiménez‐Gómez,

Plant nutrient uptake and metabolism

News & Views14 April 2020free access SlHAK20: a new player in plant salt tolerance Yanli Xiang Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, Versailles, France Search for more papers by this author José M Jiménez-Gómez Corresponding Author [email protected] orcid.org/0000-0002-5033-7192 Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, Versailles, France Search for more papers by this author Yanli Xiang Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, Versailles, France Search for more papers by this author José M Jiménez-Gómez Corresponding Author [email protected] orcid.org/0000-0002-5033-7192 Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, Versailles, France Search for more papers by this author Author Information Yanli Xiang1 and José M Jiménez-Gómez *,1 1Institut Jean-Pierre Bourgin, INRAE, AgroParisTech, Université Paris-Saclay, Versailles, France EMBO J (2020)39:e104997https://doi.org/10.15252/embj.2020104997 See also: Z Wang et al (May 2020) PDFDownload PDF of article text and main figures. ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinked InMendeleyWechatReddit Figures & Info The majority of crops remain sensitive to salt stress despite the steady increase in salt concentration in agricultural soil. In this issue of The EMBO Journal, Wang et al (2020) screen hundreds of tomato accessions to identify SlHAK20 as a gene accounting for quantitative differences in salt tolerance between accessions. SlHAK20 is a potassium transporter belonging to a poorly studied clade in a large family of transporters, and its mutation induces salt susceptibility both in tomato and rice. Soil salinity is one of the leading environmental stresses affecting agriculture, causing billions of dollars in crop damages every year (Jamil et al, 2011). About 11% of the global land area is exposed to salinity, mainly due to the use of mineral fertilizers and irrigation with saline water (Kamran et al, 2020). High salt concentrations in the soil can have significant effects in crops, inhibiting plant germination, growth, and yield. These detrimental effects are caused by the excess accumulation of Na+ in the cells, inducing efflux of cytosolic K+ and Ca2+, and leading to cellular homeostasis imbalance, nutrient deficiency, oxidative stress, and cell death (Kamran et al, 2020). Most crops, including tomato, are salt sensitive. Breeding for salt tolerance has been a priority since the 1930s, with more than 18,000 existing patents invoking plant salinity tolerance (Flowers, 2004; Rao et al, 2015). The most common mechanisms that allow plants to resist salinity are osmotic stress tolerance, restriction of the entrance of toxic ions, and tissue tolerance by compartmentalization of toxic ions into vacuoles (Munns & Tester, 2008; Rao et al, 2015). Therefore, genes that can play a role in salt resistance would be typically involved in minimizing sodium and/or chloride uptake, maximizing selectivity of potassium over sodium, controlling salt flux to the shoot through the entry of ions into the xylem, reducing transpiration, or synthesizing compatible solutes (Cuartero et al, 2006). Tomato was one of the first species used to evaluate the possibility of increasing salt tolerance through crosses with its wild relatives (Lyon, 1941). While most tomato cultivars are very sensitive to salinity, many wild tomato species are salt tolerant (Bai et al, 2018). Multiple studies have tried to identify the natural alleles involved in salt tolerance in tomato using crosses between cultivated accessions and wild species (Bai et al, 2018). A general trend in these studies is a strong dependence of salinity tolerance on developmental stages (Foolad, 2004), the difficulty to accurately measure plant responses to salinity (Cuartero et al, 2006) and a complex underlying genetic architecture, where genes affecting salinity tolerance are numerous, widely distributed across the tomato genome and display medium to low heritability (Bai et al, 2018). In this issue of The EMBO Journal, Wang et al perform for the first time genome-wide association studies (GWAS) for salt tolerance in a panel of 369 tomato accessions from its closest wild relative, early domesticated types, and modern varieties. The authors measure Na+ and K+ content under salt treatment in roots and shoots in all accessions and find that Na+ contents and Na+/K+ ratios in roots are notably higher in modern cultivated tomato than in wild and pre-domesticated accessions. Wang et al then take advantage of available genome-wide polymorphisms in these accessions to perform GWAS of Na+ and K+ accumulation. The most significant association was found 86 kb upstream from SlHAK20, a member of the large HAK/KUP/KT family of potassium transporters. All modern tomato and most pre-domesticated tomato accessions carry a 6 bp deletion in the coding region of SlHAK20 that is also present in low frequency in wild tomatoes. Accessions carrying the 6 bp deletion in SlHAK20 show significantly higher root Na+/K+ ratio than accessions without the deletion. Through a series of genetics, biochemistry, and molecular biology experiments, the authors proved that SlHAK20 functions in the loading of K+ and Na+ from parenchyma cells into the xylem in roots. Under salt stress, the wild allele of SlHAK20 has higher Na+ affinity and loads more Na+ into the root xylem, therefore lowering the Na+/K+ ratio in root cells in comparison with the cultivated allele and leading to higher salt tolerance. CRISPR knockout of SlHAK20 increases Na+ concentrations in roots and renders tomato plants more sensitive to salinity, while overexpression of SlHAK20 triggered the opposite phenotype. Importantly, CRISPR knockout of the SlHAK20 homologs in rice, OsHAK4 and OsHAK17, severely affects plant biomass and survival rate under salt treatment, suggesting breeding possibilities through modification of these transporters both in dicots and monocots. The work of Wang et al exemplifies the use of natural variation to link phenotype to genotype in large gene families, such as the HAK/KUP/KT family of K+ transporters, where methods based in induced mutagenesis may fail due to redundancy, and identification of those members that are more suitable for crop improvement remains complicated (Nieves-Cordones et al, 2016). In addition, the study by Wang et al emphasizes the benefits of using a diverse set of plant species in research. The HAK/KUP/KT family is divided into five clades with wildly different number of members in each species. SlHAK20 belongs to clade IV, one of the less studied partly due to its absence in the Brassicaceae family, that includes the best-studied plant model Arabidopsis (Nieves-Cordones et al, 2016). Nevertheless, members of clade IV HAK/KUP/KT K+ transporters are present in many plant species, including dicots and monocots. Under these premises, the authors show that the role of SlHAK20 increasing salt tolerance can be translated to its homologs in rice. In summary, the work from Wang et al stands out because of the importance of its findings for agriculture, but also for its completeness, including the exploration of natural variation in salt tolerance in tomato, the identification of the gene responsible for the variation, functional characterization of the protein, and the demonstration of its value for breeding both in dicots and monocots. References Bai Y, Kissoudis C, Yan Z, Visser RGF, van der Linden G (2018) Plant behaviour under combined stress: tomato responses to combined salinity and pathogen stress. Plant J. 93: 781–793Wiley Online LibraryCASPubMedWeb of Science®Google Scholar Cuartero J, Bolarín MC, Asíns MJ, Moreno V (2006) Increasing salt tolerance in the tomato. J Exp Bot 57: 1045–1058CrossrefCASPubMedWeb of Science®Google Scholar Flowers TJ (2004) Improving crop salt tolerance. 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Annu Rev Plant Biol 59: 651–681CrossrefCASPubMedWeb of Science®Google Scholar Nieves-Cordones M, Ródenas R, Chavanieu A, Rivero RM, Martinez V, Gaillard I, Rubio F (2016) Uneven HAK/KUP/KT protein diversity among angiosperms: species distribution and perspectives. Front Plant Sci 7: 127CrossrefPubMedWeb of Science®Google Scholar Rao ES, Kadirvel P, Symonds RC, Geethanjali S, Thontadarya RN, Ebert AW (2015) Variations in DREB1A and VP1.1 genes show association with salt tolerance traits in wild tomato (Solanum pimpinellifolium). PLoS ONE 10: e0132535CrossrefPubMedWeb of Science®Google Scholar Wang Z, Hong Y, Zhu G, Li Y, Niu Q, Yao J, Hua K, Bai J, Zhu Y, Shi H et al (2020) Loss of salt tolerance during tomato domestication conferred by variation in a Na(+)/K(+) transporter. EMBO J https://doi.org/10.15252/embj.2019103256Wiley Online LibraryGoogle Scholar Previous ArticleNext Article Read MoreAbout the coverClose modalView large imageVolume 39,Issue 10,18 May 2020This month's cover highlights the articles Rhomboid intramembrane protease YqgP licenses bacterial membrane protein quality control as adaptor of FtsH AAA protease by Jakub Began, Baptiste Cordier, Thierry Doan, Kvido Strisovsky and colleagues, and Bacterial rhomboid proteases mediate quality control of orphan membrane proteins by Guangyu Liu, Adam Grieve, Rachel Exley, Christoph Tang and colleagues. The articles show that rhomboid proteases sense and help degrade faulty and orphan membrane proteins in bacteria, which is conceptually analogous to the role of the rhomboid-like proteins Derlins in ER-associated degradation in eukaryotes. (Cover art by Oliver Hoeller, www.oliverhoeller.com). Volume 39Issue 1018 May 2020In this issue ReferencesRelatedDetailsLoading ...