Overexpression of phosphatidylserine synthase IbPSS1 affords cellular Na+ homeostasis and salt tolerance by activating plasma membrane Na+/H+ antiport activity in sweet potato roots

Yicheng Yu , Ying Xuan , Xiaofeng Bian , Lei Zhang , Zhiyuan Pan , Meng Kou , Qinghe Cao , Zhonghou Tang , Qiang Li , Daifu Ma , Zongyun Li , Jian Sun

Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) : 131

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Horticulture Research ›› 2020, Vol. 7 ›› Issue (1) :131 DOI: 10.1038/s41438-020-00358-1
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Overexpression of phosphatidylserine synthase IbPSS1 affords cellular Na+ homeostasis and salt tolerance by activating plasma membrane Na+/H+ antiport activity in sweet potato roots
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Abstract

Phosphatidylserine synthase (PSS)-mediated phosphatidylserine (PS) synthesis is crucial for plant development. However, little is known about the contribution of PSS to Na+ homeostasis regulation and salt tolerance in plants. Here, we cloned the IbPSS1 gene, which encodes an ortholog of Arabidopsis AtPSS1, from sweet potato (Ipomoea batatas (L.) Lam.). The transient expression of IbPSS1 in Nicotiana benthamiana leaves increased PS abundance. We then established an efficient Agrobacterium rhizogenes-mediated in vivo root transgenic system for sweet potato. Overexpression of IbPSS1 through this system markedly decreased cellular Na+ accumulation in salinized transgenic roots (TRs) compared with adventitious roots. The overexpression of IbPSS1 enhanced salt-induced Na+/H+ antiport activity and increased plasma membrane (PM) Ca2+-permeable channel sensitivity to NaCl and H2O2 in the TRs. We confirmed the important role of IbPSS1 in improving salt tolerance in transgenic sweet potato lines obtained from an Agrobacterium tumefaciens-mediated transformation system. Similarly, compared with the wild-type (WT) plants, the transgenic lines presented decreased Na+ accumulation, enhanced Na+ exclusion, and increased PM Ca2+-permeable channel sensitivity to NaCl and H2O2 in the roots. Exogenous application of lysophosphatidylserine triggered similar shifts in Na+ accumulation and Na+ and Ca2+ fluxes in the salinized roots of WT. Overall, this study provides an efficient and reliable transgenic method for functional genomic studies of sweet potato. Our results revealed that IbPSS1 contributes to the salt tolerance of sweet potato by enabling Na+ homeostasis and Na+ exclusion in the roots, and the latter process is possibly controlled by PS reinforcing Ca2+ signaling in the roots.

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Yicheng Yu, Ying Xuan, Xiaofeng Bian, Lei Zhang, Zhiyuan Pan, Meng Kou, Qinghe Cao, Zhonghou Tang, Qiang Li, Daifu Ma, Zongyun Li, Jian Sun. Overexpression of phosphatidylserine synthase IbPSS1 affords cellular Na+ homeostasis and salt tolerance by activating plasma membrane Na+/H+ antiport activity in sweet potato roots. Horticulture Research, 2020, 7 (1) : 131 DOI:10.1038/s41438-020-00358-1

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References

[1]

van Zelm, E., Zhang, Y. & Testerink, C. Salt tolerance mechanisms of plants. Annu. Rev. Plant Biol. 71, 403-433 (2020).

[2]

Yang, Y. & Guo, Y. Elucidating the molecular mechanisms mediating plant salt stress responses. New Phytol. 217, 523-539 (2018).

[3]

Sun, J. et al. H2O2 and cytosolic Ca2+ signals triggered by the PM H+-coupled transport system mediate K+/Na+ homeostasis in NaCl-stressed Populus euphratica cells . Plant Cell Environ. 33, 943-958 (2010).

[4]

Niu, M. et al. Root respiratory burst oxidase homologue-dependent H2O2 production confers salt tolerance on a grafted cucumber by controlling Na+ exclusion and stomatal closure . J. Exp. Bot. 69, 3465-3476 (2018).

[5]

Liu, Y. et al. Root-zone-specific sensitivity of K+- and Ca2+-permeable channels to H2O2 determines ion homeostasis in salinized diploid and hexaploidy Ipomoea trifida . J. Exp. Bot. 70, 1389-1405 (2019).

[6]

Ma, L. et al. NADPH oxidase AtrbohD and AtrbohF function in ROS-dependent regulation of Na+/K+ homeostasis in Arabidopsis under salt stress . J. Exp. Bot. 63, 305-317 (2012).

[7]

Higashi, Y. & Saito, K. Lipidomic studies of membrane glycerolipids in plant leaves under heat stress. Prog. Lipid Res. 75, 100990 (2019).

[8]

Hong, Y. et al. Plant phospholipases D and C and their diverse functions in stress responses. Prog. Lipid Res. 62, 55-74 (2016).

[9]

Ali, U., Li, H., Wang, X. & Guo, L. Emerging roles of sphingolipid signaling in plant response to biotic and abiotic stresses. Mol. Plant. 11, 1328-1343 (2018).

[10]

Li, L. et al. A phosphoinositide-specific phospholipase C pathway elicits stress-induced Ca2+ signals and confers salt tolerance to rice . New Phytol. 214, 1172-1187 (2017).

[11]

Wang, P. et al. Phosphatidic acid directly regulates PINOID-dependent phosphorylation and activation of the PIN-FORMED2 auxin efflux transporter in response to salt stress. Plant Cell. 31, 250-271 (2019).

[12]

Zhang, Q. et al. Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell. 24, 4555-4576 (2012).

[13]

Yu, L. et al. Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol. 188, 762-773 (2010).

[14]

Li, W. et al. Tissue-specific accumulation of pH-sensing phosphatidic acid determines plant stress tolerance. Nat. Plants 5, 1012-1021 (2019).

[15]

Guo, L. et al. Cytosolic glyceraldehyde-3-phosphate dehydrogenases interact with phospholipase Dδ to transduce hydrogen peroxide signals in the Arabidopsis response to stress. Plant Cell. 24, 2200-2212 (2012).

[16]

Jiang, Z. et al. Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx . Nature 572, 341-346 (2019).

[17]

Platre, M. P. et al. A combinatorial lipid code shapes the electrostatic landscape of plant endomembranes. Dev. Cell. 45, 465-480 (2018).

[18]

Yang, X. et al. Phosphatidylserine synthase regulates cellular homeostasis through distinct metabolic mechanisms. PLoS Genet. 5, e1008548 (2019).

[19]

Yamaoka, Y. et al. Phosphatidylserine synthase 1 is required for microspore development in Arabidopsis thaliana. Plant J. 67, 648-661 (2011).

[20]

Liu, C. et al. Phosphatidylserine synthase 1 is required for inflorescence meristem and organ development in Arabidopsis. J. Integr. Plant Biol. 55, 682-695 (2013).

[21]

Rani, M. H. et al. ES5 is involved in the regulation of phosphatidylserine synthesis and impacts on early senescence in rice (Oryza sativa L.). Plant Mol. Biol. 102, 501-515 (2020).

[22]

Ma, J. et al. Phosphatidylserine synthase controls cell elongation especially in the uppermost internode in rice by regulation of exocytosis. PLoS ONE 11, e0153119 (2016).

[23]

Zhu, L. et al. Identification and characterization of SHORTENED UPPERMOST INTERNODE 1, a gene negatively regulating uppermost internode elongation in rice. Plant Mol. Biol. 77, 475-487 (2011).

[24]

Platre, M. P. et al. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364, 57-62 (2019).

[25]

Yu, Y. et al. Involvement of phosphatidylserine and triacylglycerol in the response of sweet potato leaves to salt stress. Front Plant Sci. 10, 1086 (2019).

[26]

Meng, D. et al. Development of an efficient root transgenic system for pigeon pea and its application to other important economically plants. Plant Biotechnol. J. 17, 1804-1813 (2019).

[27]

Sun, J. et al. NaCl-induced alternations of cellular and tissue ion fluxes in roots of salt-resistant and salt sensitive poplar species. Plant Physiol. 149, 1141-1153 (2009).

[28]

Cuin, T. A. et al. Assessing the role of root plasma membrane and tonoplast Na+/H+ exchangers in salinity tolerance in wheat: in planta quantification methods . Plant Cell Environ. 34, 947-961 (2011).

[29]

Wu, H. et al. Root vacuolar Na+ sequestration but not exclusion from uptake correlates with barley salt tolerance . Plant J. 100, 55-67 (2019).

[30]

Liu, Q. Improvement for agronomically important traits by gene engineering in sweet potato. Breed. Sci. 67, 15-26 (2017).

[31]

Gomes, C., Dupas, A., Pagano, A., Grima-Pettenati, J. & Paiva, J. A. P. Hairy root transformation: A useful tool to explore gene function and expression in salix spp. recalcitrant to transformation. Front Plant Sci. 10, 1427 (2019).

[32]

Matthus, E. et al. DORN1/P2K1 and purino-calcium signalling in plants: making waves with extracellular ATP. Ann. Bot. 124, 1227-1242 (2020).

[33]

Pan, Y. et al. Dynamic interactions of plant CNGC subunits and calmodulins drive oscillatory Ca2+ channel activities . Dev. Cell. 48, 710-725 (2019).

[34]

Ron, M. et al. Hairy root transformation using Agrobacterium rhizogenes as a tool for exploring cell type-specific gene expression and function using tomato as a model. Plant Physiol. 166, 455-469 (2014).

[35]

Butler, N. M., Jansky, S. H. & Jiang, J. First generation genome editing in potato using hairy root transformation. Plant Biotechnol. J. https://doi.org/10.1111/pbi.13376. (2020)

[36]

Ming., M. et al. CRISPR-Cas12b enables efficient plant genome engineering. Nat. Plants 6, 202-208 (2020).

[37]

Kasamo, K. Mechanism for the activation of plasma membrane H+-ATPase from rice (Oryza sativa L.) culture cells by molecular species of a phospholipid . Plant Physiol. 93, 1049-1052 (1990).

[38]

Demidchik, V., Shabala, S., Isayenkov, S., Cuin, T. A. & Pottosin, I. Calcium transport across plant membranes: mechanisms and functions. New Phytol. 220, 49-69 (2018).

[39]

Sarabia, L. D. et al. Comparative spatial lipidomics analysis reveals cellular lipid remodelling in different developmental zones of barley roots in response to salinity. Plant Cell Environ. 43, 327-343 (2019).

[40]

Zhang, X., Xu, Y. & Huang, B. Lipidomic reprogramming associated with drought stress priming-enhanced heat tolerance in tall fescue (Festuca arundinacea). Plant Cell Environ. 42, 947-958 (2019).

[41]

Laohavisit, A. & Davies, J. M. Annexins. New Phytol. 89, 40-53 (2011).

[42]

Laohavisit, A. et al. Salinity-induced calcium signaling and root adaptation in Arabidopsis require the calcium regulatory protein annexin1. Plant Physiol. 163, 253-262 (2013).

[43]

Richards, S. L. et al. Annexin 1 regulates the H2O2-induced calcium signature in Arabidopsis thaliana roots . Plant J. 77, 136-145 (2014).

[44]

Ma, L. et al. The SOS2-SCaBP8 complex generates and fine-tunes an AtANN4-dependent calcium signature under salt stress. Dev. Cell. 48, 697-709 (2019).

[45]

Lee, S. et al. Proteomic identification of annexins, calcium-dependent membrane binding protein that mediate osmotic stress and abscisic acid signal transduction in Arabidopsis. Plant Cell. 16, 1378-1391 (2004).

[46]

Mu, C., Zhou, L., Shan, L., Li, F. & Li, Z. Phosphatase GhDsPTP3a interacts with annexin protein GhANN8b to reversely regulate salt tolerance in cotton (Gossypium spp.). New Phytol. 223, 1856-1872 (2019).

[47]

Kurland, R., Newton, C., Nir, S. & Papahadjopoulos, D. Specificity of Na+ binding to phosphatidylserine vesicles from a23Na NMR relaxation rate study . Biochim. Biophys. Acta. 551, 137-147 (1979).

[48]

Yang, Z. et al. Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nat. Commun. 10, 1199 (2019).

[49]

Kim, S. H., Ahn, Y. O., Ahn, M. J., Lee, H. S. & Kwak, S. S. Down-regulation of β-carotene hydroxylase increases β-carotene and total carotenoids enhancing salt stress tolerance in transgenic cultured cells of sweet potato. Phytochemistry 74, 69-78 (2012).

[50]

Yu, Y. et al. Melatonin stimulated triacylglycerol breakdown and energy turnover under salinity stress contributes to the maintenance of plasma membrane H+-ATPase activity and K+/Na+ homeostasis in sweet potato . Front Plant Sci. 9, 256 (2018).

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