Abstract
Main conclusion
A lncRNA MtCIR1 negatively regulates the response to salt stress in Medicago truncatula seed germination by modulating seedling growth and ABA metabolism and signaling by enhancing Na+ accumulation.
Abstract
Increasing evidence suggests that long non-coding RNAs (lncRNAs) are involved in the regulation of plant tolerance to varying abiotic stresses. A large number of lncRNAs that are responsive to abiotic stress have been identified in plants; however, the mechanisms underlying the regulation of plant responses to abiotic stress by lncRNAs are largely unclear. Here, we functionally characterized a salt stress-responsive lncRNA derived from the leguminous model plant M. truncatula, referred to as MtCIR1, by expressing MtCIR1 in Arabidopsis thaliana in which no such homologous sequence was observed. Expression of MtCIR1 rendered seed germination more sensitive to salt stress by enhanced accumulation of abscisic acid (ABA) due to suppressing the expression of the ABA catabolic enzyme CYP707A2. Expression of MtCIR1 also suppressed the expression of genes associated with ABA receptors and signaling. The ABA-responsive gene AtPGIP2 that was involved in degradation of cell wall during seed germination was up-regulated by expressing MtCIR1. On the other hand, expression of MtCIR1 in Arabidopsis thaliana enhanced foliar Na+ accumulation by down-regulating genes encoding Na+ transporters, thus rendering the transgenic plants more sensitive to salt stress. These results demonstrate that the M. truncatula lncRNA MtCIR1 negatively regulates salt stress response by targeting ABA metabolism and signaling during seed germination and foliar Na+ accumulation by affecting Na+ transport under salt stress during seedling growth. These novel findings would advance our knowledge on the regulatory roles of lncRNAs in response of plants to salt stress.
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All data generated or analyzed Science and Technology Department of Inner Mongolia Autonomous Region (grant number 2021ZD004502; 2021GG0372) during this study are included in this published article and its supplementary information files.
References
Alboresi A, Gestin C, Leydecker MT, Bedu M, Meyer C, Truong HN (2005) Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ 28:500–512. https://doi.org/10.1111/j.1365-3040.2005.01292.x
Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258. https://doi.org/10.1126/science.285.5431.1256
Ariel F, Romero-Barrios N, Jégu T, Benhamed M, Crespi M (2015) Battles and hijacks: noncoding transcription in plants. Trends Plant Sci 20:362–371. https://doi.org/10.1016/j.tplants.2015.03.003
Batelli G, Verslues PE, Agius F, Qiu Q, Fujii H, Pan S, Schumaker KS, Grillo S, Zhu JK (2007) SOS2 promotes salt tolerance in part by interacting with the vaculoar H+-ATPase and upregulating its transport activity. Mol Cell Biol 27:7781–7790. https://doi.org/10.1128/MCB.00430-07
Blumwald E (2000) Sodium transport and salt tolerance in plants. Curr Opin Cell Biol 12:431–434. https://doi.org/10.1016/S0955-0674(00)00112-5
Chen M, Wang CL, Bao H, Chen H, Wang YW (2016) Genome-wide identification and characterization of novel lncRNAs in Populus under nitrogen deficiency. Mol Genet Genomics 291:1663–1680. https://doi.org/10.1007/s00438-016-1210-3
Cheng Y, Tian QY, Zhang WH (2016) Glutamate receptors are involved in mitigating effects of amino acids on seed germination of Arabidopsis thaliana under salt stress. Environ Exp Bot 130:68–78. https://doi.org/10.1016/j.envexpbot.2016.05.004
Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. https://doi.org/10.1046/j.1365-313x.1998.00343.x
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122
Deng F, Zhang X, Wang W, Yuan R, Shen F (2018) Identification of Gossypium hirsutum long non-coding RNAs (lncRNAs) under salt stress. BMC Plant Biol 18:23. https://doi.org/10.1186/s12870-018-1238-0
Ferrari S, Vairo D, Ausubel FM, Cervone F, De Lorenzo G (2002) Tandemly duplicated Arabidopsis genes that encode polygalacturonase inhibiting proteins are regulated coordinately by different signal transduction pathways in response to fungal infection. Plant Cell 15:93–106. https://doi.org/10.1105/tpc.005165
Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytol 171:501–523. https://doi.org/10.1111/j.1469-8137.2006.01787.x
Finkelstein R, Gampala SSL, Lynch TJ, Thomas TL, Rock CD (2005) Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol Biol 59:253–267. https://doi.org/10.1007/s11103-005-8767-2
Fu JH, Chu JF, Sun XH, Wang JD, Yan CY (2012) Simple, rapid, and simultaneous assay of multiple carboxyl containing phytohormones in wounded tomatoes by UPLC-MS/MS using single SPE purification and isotope dilution. Anal Sci 28:1081–1087. https://doi.org/10.2116/analsci.28.1081
Guo JJ, Yang XH, Weston DJ, Chen JG (2011) Abscisic acid receptors: past, present and future. J Integr Plant Biol 53:469–479. https://doi.org/10.1111/j.1744-7909.2011.01044.x
Holbrook NM, Shashidhar V, James RA, Rana M (2002) Stomatal control in tomato with ABA-deficient roots: response of grafted plants to soil drying. J Exp Bot 373:1503–1514. https://doi.org/10.1093/jexbot/53.373.1503
Horie T, Schroeder JI (2004) Sodium transporters in plants. Diverse genes and physiological functions. Plant Physiol 136:2457–2462. https://doi.org/10.1104/pp.104.046664
Huanca-Mamani W, Arias-Carrasco R, Cardena-Ninasivincha S, Rojas-Herrera M, Sepulveda-Hermosilla G, Caris-Maldonado JS, Bastias E, Maracaja-Coutinho V (2018) Long non-coding RNAs responsive to salt and boron stress in the hyper-arid Lluteno maize from Atacama Desert. Genes 9(170):170. https://doi.org/10.3390/genes9030170
Huang Y, Feng CZ, Ye Q, Wu WH, Chen YF (2016) Arabidopsis WRKY6 transcription factor acts as a positive regulator of abscisic acid signaling during seed germination and early seedling development. PLoS Genet 12:e1005833. https://doi.org/10.1371/journal.pgen.1005833
Ishitani M, Liu JP, Halfter U, Kim CS, Shi WM, Zhu JK (2000) SOS3 function in plant salt tolerance requires N-myristoylation and calcium binding. Plant Cell 12:1667–1678. https://doi.org/10.1105/tpc.12.9.1667
Jiang ZH, Zhou XP, Tao M et al (2019) Plant cell-surface GIPC sphingolipids sense salt to trigger Ca2+ influx. Nature 572:341–346. https://doi.org/10.1038/s41586-019-1449-z
Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594. https://doi.org/10.1016/j.tplants.2015.06.008
Kalunke RM, Tundo S, Benedetti M, Cervone F, De Lorenzo G, D’Ovidio R (2015) An update on polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein that protects crop plants against pathogens. Front Plant Sci 6:146. https://doi.org/10.3389/fpls.2015.00146
Kanai M, Nishimura M, Hayashi M (2010) A peroxisomal ABC transporter promotes seed germination by inducing pectin degradation under the control of ABI5. Plant J 62:936–947. https://doi.org/10.1111/j.1365-313X.2010.04205.x
Ketehouli T, Carther KFI, Noman M, Wang FW, Li XW, Li HY (2019) Adaptation of plants to salt stress: characterization of Na+ and K+ transporters and role of CBL gene family in regulating salt stress response. Agronomy 9:687. https://doi.org/10.3390/agronomy9110687
Khandelwal A, Cho SH, Marella H, Sakata Y, Perroud PF, Pan A, Quatrano RS (2010) Role of ABA and ABI3 in desiccation tolerance. Science 327:546–548. https://doi.org/10.1126/science.1183672
Kim TH, Böhmer M, Hu H, Nishimura N, Schroeder JI (2010) Guard cell signal transduction network: advances in understanding abscisic acid, CO2, and Ca2+ signaling. Annu Rev Plant Biol 61:561–591. https://doi.org/10.1146/annurev-arplant-042809-112226
Koornneef M, Bentsink L, Hilhorst H (2002) Seed dormancy and germination. Curr Opin Plant Biol 5:33–36. https://doi.org/10.1016/S1369-5266(01)00219-9
Kornienko AE, Guenzl PM, Barlow DP, Pauler FM (2013) Gene regulation by the act of long non-coding RNA transcription. BMC Biol 11:59. https://doi.org/10.1186/1741-7007-11-59
Kumar M, Kesawat MS, Ali A, Lee SC, Gill SS, Kim HU (2019) Integration of abscisic acid signaling with other signaling pathways in plant stress responses and development. Plants 8:592. https://doi.org/10.3390/plants8120592
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450 CYP707A encodes ABA 8-hydroxylases: key enzymes in ABA catabolism. EMBO J 23:1647–1656. https://doi.org/10.1038/sj.emboj.7600121
Laurie S, Feeney KA, Maathuis FJM, Heard PJ, Brown SJ, Leigh RA (2002) A role for HKT1 in sodium uptake by wheat roots. Plant J 32:139–149. https://doi.org/10.1046/j.1365-313X.2002.01410.x
Li L, Eichten SR, Shimizu R et al (2014) Genome-wide discovery and characterization of maize long non-coding RNAs. Genome Biol 15:R40. https://doi.org/10.1186/gb-2014-15-2-r40
Li N, Wang ZY, Wang BK, Wang J, Xu RQ, Yang T, Huang SY, Wang H, Yu QH (2022) Identification and characterization of long non-coding RNA in tomato roots under salt stress. Front Plant Sci 13:834027. https://doi.org/10.3389/fpls.2022.834027
Liu JP, Ishitani M, Halfter U, Kim CS, Zhu JK (2000) The Arabidopsis thaliana SOS2 gene encodes a protein kinase that is required for salt tolerance. Proc Natl Acad Sci USA 97:3730–3734. https://doi.org/10.1073/pnas.97.7.3730
Liu J, Wang H, Chua NH (2015) Long noncoding RNA transcriptome of plants. Plant Biotech J 13:319–328
Liu X, Hu PW, Huang MK, Tang Y, Li Y, Li L, Hou XL (2016) The NF-YC–RGL2 module integrates GA and ABA signaling to regulate seed germination in Arabidopsis. Nature Comm 7:12768–12782. https://doi.org/10.1038/ncomms12768
Lopez-Molina L, Mongrand S, McLachlin DT, Chait BT, Chua NH (2002) ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J 32:317–328. https://doi.org/10.1046/j.1365-313x.2002.01430.x
Luo X, Bai X, Sun XL, Zhu D, Liu BH, Ji W, Cai H, Cao L, Wu J, Hu MR, Liu X, Tang LL, Zhu YM (2013) Expression of wild soybean WRKY20 in Arabidopsis enhances drought tolerance and regulates ABA signalling. J Exp Bot 64:2155–2169. https://doi.org/10.1093/jxb/ert073
Mansour MMF, Salama KHA, Al-Mutawa MM (2003) Transport proteins and salt tolerance in plants. Plant Sci 164:891–900. https://doi.org/10.1016/S0168-9452(03)00109-2
Manz B, Müller K, Kucera B, Volke F, Leubner-Metzger G (2005) Water uptake and distribution in germinating tobacco seeds investigated in vivo by nuclear magnetic resonance imaging. Plant Physiol 138:1538–1551. https://doi.org/10.1104/pp.105.061663
Miao C, Xiao L, Hua K, Zou C, Zhao Y, Bressan RA, Zhu JK (2018) Mutations in a subfamily of abscisic acid receptor genes promote rice growth and productivity. Proc Natl Acad Sci USA 115:6058–6063. https://doi.org/10.1073/pnas.1804774115
Miyazono KI, Miyakawa T, Sawano Y, Kubota K, Kang HJ, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira KS, Kazuko Yamaguchi-Shinozaki Y, Tanokura M (2009) Structural basis of abscisic acid signalling. Nature 462:609–614. https://doi.org/10.1038/nature08583
Munemasa S, Hauser F, Park J, Waadt R, Brandt B, Schroeder JI (2015) Mechanisms of abscisic acid-mediated control of stomatal aperture. Curr Opin Plant Biol 28:154–162. https://doi.org/10.1016/j.pbi.2015.10.010
Nakashima K, Yamaguchi-Shinozaki K (2013) ABA signaling in stress-response and seed development. Plant Cell Rep 232:959–970. https://doi.org/10.1007/s00299-013-1418-1
Nonogaki H, Bassel GW, Bewley JD (2010) Germination-still a mystery. Plant Sci 179:574–581. https://doi.org/10.1016/j.plantsci.2010.02.010
Park SY, Fung P, Nishimura N et al (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/ PYL family of START proteins. Science 324:1068–1071. https://doi.org/10.1126/science.1173041
Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136:629–641. https://doi.org/10.1016/j.cell.2009.02.006
Qin T, Zhao H, Cui P, Albesher N, Xiong LM (2017) A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 75:1321–1336. https://doi.org/10.1104/pp.17.00574
Qiu QS, Guo Y, Dietrich MA, Schumaker KS, Zhu JK (2002) Regulation of SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2 and SOS3. Proc Natl Acad Sci USA 99:8436–8441. https://doi.org/10.1073/pnas.122224699
Rajjou L, Duval M, Gallardo K, Catusse J, Bally J, Job C, Job D (2012) Seed germination and vigor. Annu Rev Plant Biol 63:507–533. https://doi.org/10.1146/annurev-arplant-042811-105550
Rathinam M, Rao U, Sreevathsa R (2020) Novel biotechnological strategies to combat biotic stresses: polygalacturonase inhibitor (PGIP) proteins as a promising comprehensive option. Appl Microbiol Biotechnol 104:2333–2342. https://doi.org/10.1007/s00253-020-10396-3
Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee BH, Matsumoto TK, Koiwa H, Zhu JK, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155. https://doi.org/10.1073/pnas.241501798
Sah SK, Reddy KR, Li JX (2016) Abscisic acid and abiotic stress tolerance in crop plants. Front Plant Sci 7:571. https://doi.org/10.3389/fpls.2016.00571
Shi HZ, Ishitani M, Kim C, Zhu JK (2000) The Arabidopsis thaliana salt tolerance gene SOS1 encodes a putative Na+/H+ antiporter. Proc Natl Acad Sci USA 97:6896–6901. https://doi.org/10.1073/pnas.120170197
Shinozaki K, Yamaguchi-Shinozaki K (2007) Gene networks involved in drought stress response and tolerance. J Exp Bot 58:221–227. https://doi.org/10.1093/jxb/erl164
Sunarpi HT, Motoda J et al (2005) Enhanced salt tolerance mediated by AtHKT1 transporter-induced Na unloading from xylem vessels to xylem parenchyma cells. Plant J 44:928–938. https://doi.org/10.1111/j.1365-313X.2005.02595.x
Verslues PE, Zhu JK (2007) New developments in abscisic acid perception metabolism. Curr Opin Plant Biol 10:447–452. https://doi.org/10.1016/j.pbi.2007.08.004
Vishwakarma K, Upadhyay N, Kumar N, Yadav G, Singh J, Mishra RK, Kumar V, Verma R, Upadhyayet RG, Pandeyal M, Sharma S (2017) Abscisic acid signaling and abiotic stress tolerance in plants: a review on current knowledge and future prospects. Front Plant Sci 20:161. https://doi.org/10.3389/fpls.2017.00161
Wang H, Chung PJ, Liu J, Jang IC, Kean MJ, Xu J, Chua NH (2014a) Genome-wide identification of long noncoding natural antisense transcripts and their responses to light in Arabidopsis. Genome Res 24:444–453. https://doi.org/10.1101/gr.165555.113
Wang Y, Fan X, Lin F, He G, Terzaghi W, Zhu D, Deng XW (2014b) Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc Natl Acad Sci USA 111:10359–10364. https://doi.org/10.1073/pnas.1409457111
Wang T, Tohge T, Ivakov A, Mueller-Roeber B, Fernie AR, Mutwil M, Schippers JHM, Persson S (2015a) Salt-related MYB1 coordinates abscisic acid biosynthesis and signaling during salt stress in Arabidopsis. Plant Physiol 169:1027–1041. https://doi.org/10.1104/pp.15.00962
Wang TZ, Liu M, Zhao MG, Chen RJ, Zhang WH (2015b) Identification and characterization of long non-coding RNAs involved in osmotic and salt stress in Medicago truncatula using genome-wide high-throughput sequencing. BMC Plant Biol 15:131. https://doi.org/10.1186/s12870-015-0530-5
Wang ZJ, Ren ZY, Cheng CH et al (2020) Counteraction of ABA-mediated inhibition of seed germination and seedling establishment by ABA signaling terminator in Arabidopsis. Mol Plant 13:1284–1297. https://doi.org/10.1016/j.molp.2020.06.011
Wilkinson S, Davies WJ (2002) ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ 25:195–210. https://doi.org/10.1046/j.0016-8025.2001.00824.x
Wu RN, Wang H, Yang CC, Wang ZY, Wu YJ (2017) Construction of lncRNA At5NC056820 overexpression vector in Arabidopsis thaliana and study on drought resistance of transgenic plants. Acta Bot Boreali-Occidentalia Sin 37:1904–1909
Wu J, Liu CX, Liu ZG, Li S, Li DD, Liu SY, Huang XQ, Liu SK, Yukawa YS (2019) Pol III-dependent cabbage BoNR8 long ncRNA affects seed germination and growth in Arabidopsis. Plant Cell Physiol 60:421–435. https://doi.org/10.1093/pcp/pcy220
Xu ZY, Kim DH, Hwang I (2013) ABA homeostasis and signaling involving multiple subcellular compartments and multiple receptors. Plant Cell Rep 32:807–813. https://doi.org/10.1007/s00299-013-1396-3
Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803. https://doi.org/10.1146/annurev.arplant.57.032905.105444
Yokoi S, Quintero FJ, Cubero B, Ruiz MT, Bressan RA, Hasegawa PM, Pardo JM (2002) Differential expression and function of Arabidopsis thaliana NHX Na+/H+ antiporters in the salt stress response. Plant J 30:529–539. https://doi.org/10.1046/j.1365-313X.2002.01309.x
Yu JN, Huang J, Wang ZN, Zhang JS, Chen SY (2008) A Na+/H+ antiporter gene from wheat plays an important role in stress tolerance. J Biosci 32:1153–1161. https://doi.org/10.1007/s12038-007-0117-x
Yuan K, Rashotte AM, Wysocka-Diller JW (2011) ABA and GA signaling pathways interact and regulate seed germination and seedling development under salt stress. Acta Physiol Plant 33:261–271. https://doi.org/10.1007/s11738-010-0542-6
Zhang X, Garreton V, Chua NH (2005) The AIP2 E3 ligase acts as a novel negative regulator of ABA signaling by promoting ABI3 degradation. Genes Develop 19:1532–1543. https://doi.org/10.1101/gad.1318705
Zhang Z, Hu X, Zhang Y, Miao Z, Xie C, Meng X, Deng J, Wen J, Mysore KS, Frugier F, Wang T, Dong J (2016) Opposing control by transcription factors MYB61 and MYB3 increases freezing tolerance by relieving C-Repeat binding factor suppression. Plant Physiol 172:1306–1323. https://doi.org/10.1104/pp.16.00051
Zhang XP, Dong J, Deng FN, Wang W, Cheng YY, Song LR, Hu MJ, Shen J, Xu QJ, Shen FF (2019) The long non-coding RNA lncRNA973 is involved in cotton response to salt stress. BMC Plant Biol 19:459. https://doi.org/10.1186/s12870-019-2088-0
Zhang XP, Shen J, Xu QJ, Dong J, Song LR, Wang W, Shen FF (2021) Long noncoding RNA lncRNA354 functions as a competing endogenous RNA of miR160b to regulate ARF genes in response to salt stress in upland cotton. Plant Cell Environ 44:3302–3321. https://doi.org/10.1111/pce.14133
Zhao X, Li J, Lian B, Gu H, Li Y, Qi Y (2018) Global identification of Arabidopsis lncRNAs reveals the regulation of MAF4 by a natural antisense RNA. Nature Commu 9:5056. https://doi.org/10.1038/s41467-018-07500-7
Zhao MG, Wang TZ, Sun TY, Yu XX, Tian R, Zhang WH (2020) Identification of tissue-specific and cold-responsive lncRNAs in Medicago truncatula by high-throughput RNA sequencing. BMC Plant Biol 20:99. https://doi.org/10.1186/s12870-020-2301-1
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71. https://doi.org/10.1016/S1360-1385(00)01838-0
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273. https://doi.org/10.1146/annurev.arplant.53.091401.143329
Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324. https://doi.org/10.1016/j.cell.2016.08.029
Zhu JK, Liu J, Xiong L (1998) Genetic analysis of salt tolerance in Arabidopsis. Evidence for a critical role of potassium nutrition. Plant Cell 10:1181–1191. https://doi.org/10.1105/tpc.10.7.1181
Zhu QH, Stephen S, Taylor J, Helliwell CA, Wang MB (2013) Long noncoding RNAs responsive to Fusarium oxysporum infection in Arabidopsis thaliana. New Phytol 201:574–584. https://doi.org/10.1111/nph.12537
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We thank the technical support from the Test Centre of State Key Laboratory of Vegetation and Environmental Change.
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Science and Technology Program of Inner Mongolia, China (2021ZD004502; 2021GG0372), the National Natural Science Foundation of China (31671270).
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Tian, R., Sun, X., Liu, C. et al. A Medicago truncatula lncRNA MtCIR1 negatively regulates response to salt stress. Planta 257, 32 (2023). https://doi.org/10.1007/s00425-022-04064-1
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DOI: https://doi.org/10.1007/s00425-022-04064-1