Combined transcriptomics and metabolomics analysis reveals salinity stress specific signaling and tolerance responses in the seagrass Zostera japonica.
Zostera japonica
Antioxidant system
Cell wall remodeling
Ion transport
Osmolytes
Saline stress
Journal
Plant cell reports
ISSN: 1432-203X
Titre abrégé: Plant Cell Rep
Pays: Germany
ID NLM: 9880970
Informations de publication
Date de publication:
30 Jul 2024
30 Jul 2024
Historique:
received:
08
05
2024
accepted:
18
07
2024
medline:
31
7
2024
pubmed:
31
7
2024
entrez:
30
7
2024
Statut:
epublish
Résumé
Multiple regulatory pathways of Zostera japonica to salt stress were identified through growth, physiological, transcriptomic and metabolomic analyses. Seagrasses are marine higher submerged plants that evolved from terrestrial monocotyledons and have fully adapted to the high saline seawater environment during the long evolutionary process. As one of the seagrasses growing in the intertidal zone, Zostera japonica not only has the ability to quickly adapt to short-term salt stress but can also survive at salinities ranging from the lower salinity of the Yellow River estuary to the higher salinity of the bay, making it a good natural model for studying the mechanism underlying the adaptation of plants to salt stress. In this work, we screened the growth, physiological, metabolomic, and transcriptomic changes of Z. japonica after a 5-day exposure to different salinities. We found that high salinity treatment impeded the growth of Z. japonica, hindered its photosynthesis, and elicited oxidative damage, while Z. japonica increased antioxidant enzyme activity. At the transcriptomic level, hypersaline stress greatly reduced the expression levels of photosynthesis-related genes while increasing the expression of genes associated with flavonoid biosynthesis. Meanwhile, the expression of candidate genes involved in ion transport and cell wall remodeling was dramatically changed under hypersaline stress. Moreover, transcription factors signaling pathways such as mitogen-activated protein kinase (MAPK) were also significantly influenced by salt stress. At the metabolomic level, Z. japonica displayed an accumulation of osmolytes and TCA mediators under hypersaline stress. In conclusion, our results revealed a complex regulatory mechanism in Z. japonica under salt stress, and the findings will provide important guidance for improving salt resistance in crops.
Identifiants
pubmed: 39080075
doi: 10.1007/s00299-024-03292-x
pii: 10.1007/s00299-024-03292-x
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
203Subventions
Organisme : National Natural Science Foundation of China
ID : 42206117
Informations de copyright
© 2024. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Ahanger MA, Tomar NS, Tittal M, Argal S, Agarwal RM (2017) Plant growth under water/salt stress: ROS production; antioxidants and significance of added potassium under such conditions. Physiol Mol Biol Plants 23(4):731–744. https://doi.org/10.1007/s12298-017-0462-7
doi: 10.1007/s12298-017-0462-7
pubmed: 29158624
pmcid: 5671444
Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiol 130(3):1443–1453. https://doi.org/10.1104/pp.011114
doi: 10.1104/pp.011114
pubmed: 12428009
pmcid: 166663
Apostoloumi C, Malea P, Kevrekidis T (2021) Principles and concepts about seagrasses: towards a sustainable future for seagrass ecosystems. Mar Pollut Bull 173:112936. https://doi.org/10.1016/j.marpolbul.2021.112936
doi: 10.1016/j.marpolbul.2021.112936
pubmed: 34562848
Arai M, Pak JY, Nomura K, Nitta T (1991) Seawater-resistant, non-spherical protoplasts from seagrass leaves. Physiol Plant 83(4):551–559
doi: 10.1111/j.1399-3054.1991.tb02467.x
Athar H-R, Zulfiqar F, Moosa A, Ashraf M, Zafar ZU, Zhang L, Ahmed N, Kalaji HM, Nafees M, Hossain MA, Islam MS, El Sabagh A, Siddique KHM (2022) Salt stress proteins in plants: an overview. Front Plant Sci 13:999058
doi: 10.3389/fpls.2022.999058
pubmed: 36589054
pmcid: 9800898
Bahieldin A, Atef A, Sabir JSM, Gadalla NO, Edris S, Alzohairy AM, Radhwan NA, Baeshen MN, Ramadan AM, Eissa HF, Hassan SM, Baeshen NA, Abuzinadah O, Al-Kordy MA, El-Domyati FM, Jansen RK (2015) RNA-Seq analysis of the wild barley (H. spontaneum) leaf transcriptome under salt stress. C R Biol. https://doi.org/10.1016/j.crvi.2015.03.010
doi: 10.1016/j.crvi.2015.03.010
pubmed: 26318047
Baillo EH, Kimotho RN, Zhang Z, Xu P (2019) Transcription factors associated with abiotic and biotic stress tolerance and their potential for crops improvement. Genes 10(10):771. https://doi.org/10.3390/genes10100771
doi: 10.3390/genes10100771
pubmed: 31575043
pmcid: 6827364
Barhoumi Z, Djebali W, Chaïbi W, Abdelly C, Smaoui A (2007) Salt impact on photosynthesis and leaf ultrastructure of Aeluropus littoralis. J Plant Res 120(4):529–537. https://doi.org/10.1007/s10265-007-0094-z
doi: 10.1007/s10265-007-0094-z
pubmed: 17534691
Ben KR, Abdelly C, Savouré A (2014) How reactive oxygen species and proline face stress together. Plant Physiol Biochem 80:278–284. https://doi.org/10.1016/j.plaphy.2014.04.007
doi: 10.1016/j.plaphy.2014.04.007
Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65(5):1241–1257. https://doi.org/10.1093/jxb/ert430
doi: 10.1093/jxb/ert430
pubmed: 24368505
Boursiac Y, Chen S, Luu D-T, Sorieul M, van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots molecular and cellular features of aquaporin expression. Plant Physiol. https://doi.org/10.1104/pp.105.065029
doi: 10.1104/pp.105.065029
pubmed: 16183846
pmcid: 1255996
Breś W, Bandurska H, Kupska A, Niedziela J, Frąszczak B (2015) Responses of pelargonium Pelargonium × hortorum L.H. Bailey to long-term salinity stress induced by treatment with different NaCl doses. Acta Physiol Plant 38(1):26. https://doi.org/10.1007/s11738-015-2048-8
doi: 10.1007/s11738-015-2048-8
Cambridge ML, Zavala-Perez A, Cawthray GR, Mondon J, Kendrick GA (2017) Effects of high salinity from desalination brine on growth, photosynthesis, water relations and osmolyte concentrations of seagrass Posidonia australis. Mar Pollut Bull 115(1):252–260. https://doi.org/10.1016/j.marpolbul.2016.11.066
doi: 10.1016/j.marpolbul.2016.11.066
pubmed: 27989371
Cavusoglu E, Sari U, Tiryaki I (2023) Genome-wide identification and expression analysis of Na
doi: 10.1002/pld3.543
pubmed: 37965196
pmcid: 10641485
Chang W, Liu X, Zhu J, Fan W, Zhang Z (2016) An aquaporin gene from halophyte Sesuvium portulacastrum, SpAQP1, increases salt tolerance in transgenic tobacco. Plant Cell Rep 35(2):385–395. https://doi.org/10.1007/s00299-015-1891-9
doi: 10.1007/s00299-015-1891-9
pubmed: 26581952
Cheeseman JM (1988) Mechanisms of salinity tolerance in plants. Plant Physiol 87(3):547–550. https://doi.org/10.1104/pp.87.3.547
doi: 10.1104/pp.87.3.547
pubmed: 16666181
pmcid: 1054794
Chen J, Zang Y, Shang S, Liang S, Zhu M, Wang Y, Tang X (2021) Comparative chloroplast genomes of Zosteraceae species provide adaptive evolution insights into seagrass. Front Plant Sci. https://doi.org/10.3389/fpls.2021.741152
doi: 10.3389/fpls.2021.741152
pubmed: 35399196
pmcid: 10305780
Colin L, Ruhnow F, Zhu J-K, Zhao C, Zhao Y, Persson S (2022) The cell biology of primary cell walls during salt stress. Plant Cell 35(1):201–217. https://doi.org/10.1093/plcell/koac292
doi: 10.1093/plcell/koac292
pmcid: 9806596
Dabravolski SA, Isayenkov SV (2023) The regulation of plant cell wall organisation under salt stress. Front Plant Sci. https://doi.org/10.3389/fpls.2023.1118313
doi: 10.3389/fpls.2023.1118313
pubmed: 36968390
pmcid: 10036381
Dreyer I, Uozumi N (2011) Potassium channels in plant cells. FEBS J 278(22):4293–4303. https://doi.org/10.1111/j.1742-4658.2011.08371.x
doi: 10.1111/j.1742-4658.2011.08371.x
pubmed: 21955642
Engle KA, Amos RA, Yang J-Y, Glushka J, Atmodjo MA, Tan L, Huang C, Moremen KW, Mohnen D (2022) Multiple Arabidopsis galacturonosyltransferases synthesize polymeric homogalacturonan by oligosaccharide acceptor-dependent or de novo synthesis. Plant J 109(6):1441–1456. https://doi.org/10.1111/tpj.15640
doi: 10.1111/tpj.15640
pubmed: 34908202
Feki K, Quintero FJ, Pardo JM, Masmoudi K (2011) Regulation of durum wheat Na
doi: 10.1007/s11103-011-9787-8
pubmed: 21573979
Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu M-C, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu H-M, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca
doi: 10.1016/j.cub.2018.01.023
pubmed: 29456142
pmcid: 5894116
Fernández JA, García-Sánchez MJ, Felle HH (1999) Physiological evidence for a proton pump and sodium exclusion mechanisms at the plasma membrane of the marine angiosperm Zostera marina L. J Exp Bot 50(341):1763–1768. https://doi.org/10.1093/jxb/50.341.1763
doi: 10.1093/jxb/50.341.1763
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytol 179(4):945–963. https://doi.org/10.1111/j.1469-8137.2008.02531.x
doi: 10.1111/j.1469-8137.2008.02531.x
pubmed: 18565144
Garrote-Moreno A, McDonald A, Sherman TD, Sánchez-Lizaso JL, Heck KL, Cebrian J (2015) Short-term impacts of salinity pulses on ionic ratios of the seagrasses Thalassia testudinum and Halodule wrightii. Aquat Bot 120:315–321. https://doi.org/10.1016/j.aquabot.2014.09.011
doi: 10.1016/j.aquabot.2014.09.011
Morales M, Munné-Bosch S (2019) Malondialdehyde: facts and artifacts. Plant Physiol 180(3):1246–1250. https://doi.org/10.1104/pp.19.00405
doi: 10.1104/pp.19.00405
pubmed: 31253746
pmcid: 6752910
Geng G, Lv C, Stevanato P, Li R, Liu H, Yu L, Wang Y (2019) Transcriptome analysis of salt-sensitive and tolerant genotypes reveals salt-tolerance metabolic pathways in sugar beet. Int J Mol Sci. https://doi.org/10.3390/ijms20235910
doi: 10.3390/ijms20235910
pubmed: 31775274
pmcid: 6928841
Gigli-Bisceglia N, van Zelm E, Huo W, Lamers J, Testerink C (2022) Arabidopsis root responses to salinity depend on pectin modification and cell wall sensing. Development. https://doi.org/10.1242/dev.200363
doi: 10.1242/dev.200363
pubmed: 35574987
pmcid: 9270968
Guo Q, Meng L, Han J, Mao P, Tian X, Zheng M, Mur LAJ (2020) SOS1 is a key systemic regulator of salt secretion and K
doi: 10.1016/j.envexpbot.2020.104098
Gururani M, Venkatesh J, Tran L (2015) Regulation of photosynthesis during abiotic stress-induced photoinhibition. Mol Plant 8(9):1304–1320. https://doi.org/10.1016/j.molp.2015.05.005
doi: 10.1016/j.molp.2015.05.005
pubmed: 25997389
Hasegawa PM (2013) Sodium (Na
doi: 10.1016/j.envexpbot.2013.03.001
Henry C, Bledsoe SW, Griffiths CA, Kollman A, Paul MJ, Sakr S, Lagrimini LM (2015) Differential role for trehalose metabolism in salt-stressed Maize. Plant Physiol 169(2):1072–1089. https://doi.org/10.1104/pp.15.00729
doi: 10.1104/pp.15.00729
pubmed: 26269545
pmcid: 4587459
Hill CB, Jha D, Bacic A, Tester M, Roessner U (2013) Characterization of ion contents and metabolic responses to salt stress of different Arabidopsis AtHKT1;1 genotypes and their parental strains. Mol Plant 6(2):350–368. https://doi.org/10.1093/mp/sss125
doi: 10.1093/mp/sss125
pubmed: 23132143
Hou C, Song J, Yan J, Wang K, Li C, Yi Y (2020) Growth indicator response of Zostera japonica under different salinity and turbidity stresses in the Yellow River Estuary. China Mar Geol 424:106169. https://doi.org/10.1016/j.margeo.2020.106169
doi: 10.1016/j.margeo.2020.106169
Ji F, Tang L, Yang Z, Li Y, Wang W, Xu Y, Li S, Li X (2021) Transcriptome sequencing and comparative analysis of differentially expressed genes in the roots of Musa Paradisiaca under salt stress. Plant Biotechnol Rep 15(3):389–401. https://doi.org/10.1007/s11816-021-00683-4
doi: 10.1007/s11816-021-00683-4
Ji X, Sui C, Yu Y, Liu X, Li B, Sun Q (2022) Grape VvMAPK9 positively regulates salt tolerance in Arabidopsis and grape callus through regulating the antioxidative system. Plant Cell Tissue Organ Cult PCTOC 148(3):609–622. https://doi.org/10.1007/s11240-021-02218-9
doi: 10.1007/s11240-021-02218-9
Jiang J, Ma S, Ye N, Jiang M, Cao J, Zhang J (2017) WRKY transcription factors in plant responses to stresses. J Integr Plant Biol 59(2):86–101. https://doi.org/10.1111/jipb.12513
doi: 10.1111/jipb.12513
pubmed: 27995748
Jin Y, Jing W, Zhang Q, Zhang W (2015) Cyclic nucleotide gated channel 10 negatively regulates salt tolerance by mediating Na
doi: 10.1007/s10265-014-0679-2
pubmed: 25416933
Kaldy JE (2006) Production ecology of the non-indigenous seagrass, Dwarf Eelgrass (Zostera japonica Ascher & Graeb), in a Pacific northwest estuary. Hydrobiologia USA. https://doi.org/10.1007/s10750-005-5764-z
doi: 10.1007/s10750-005-5764-z
Kaldy JE, Shafer DJ (2013) Effects of salinity on survival of the exotic seagrass Zostera japonica subjected to extreme high temperature stress. Bot Mar 56(1):75–82. https://doi.org/10.1515/bot-2012-0144
doi: 10.1515/bot-2012-0144
Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, Li D, Li D (2011) ZmMKK4, a novel group C mitogen-activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant Cell Environ 34(8):1291–1303. https://doi.org/10.1111/j.1365-3040.2011.02329.x
doi: 10.1111/j.1365-3040.2011.02329.x
pubmed: 21477122
Kumar K, Raina SK, Sultan SM (2020) Arabidopsis MAPK signaling pathways and their cross talks in abiotic stress response. J Plant Biochem Biotechnol 29(4):700–714. https://doi.org/10.1007/s13562-020-00596-3
doi: 10.1007/s13562-020-00596-3
Lefcheck JS, Wilcox DJ, Murphy RR, Marion SR, Orth RJ (2017) Multiple stressors threaten the imperiled coastal foundation species eelgrass (Zostera marina) in Chesapeake Bay, USA. Glob Change Biol 23(9):3474–3483. https://doi.org/10.1111/gcb.13623
doi: 10.1111/gcb.13623
Li G, Santoni V, Maurel C (2014) Plant aquaporins: Roles in plant physiology. Biochim Biophys Acta BBA-Gen Subj 1840(5):1574–1582. https://doi.org/10.1016/j.bbagen.2013.11.004
doi: 10.1016/j.bbagen.2013.11.004
Li C, Ng CK-Y, Fan L-M (2015) MYB transcription factors, active players in abiotic stress signaling. Environ Exp Bot 114:80–91. https://doi.org/10.1016/j.envexpbot.2014.06.014
doi: 10.1016/j.envexpbot.2014.06.014
Li C-H, Tien H-J, Wen M-F, Yen HE (2021a) Myo-inositol transport and metabolism participate in salt tolerance of halophyte ice plant seedlings. Physiol Plant 172(3):1619–1629. https://doi.org/10.1111/ppl.13353
doi: 10.1111/ppl.13353
pubmed: 33511710
Li Y, Feng Z, Wei H, Cheng S, Hao P, Yu S, Wang H (2021b) Silencing of GhKEA4 and GhKEA12 revealed their potential functions under salt and potassium stresses in upland cotton. Front Plant Sci. https://doi.org/10.3389/fpls.2021.789775
doi: 10.3389/fpls.2021.789775
pubmed: 35281699
pmcid: 10305780
Li X, Ye G, Shen Z, Li J, Hao D, Kong W, Wang H, Zhang L, Chen J, Guo H (2023) Na
doi: 10.1016/j.envexpbot.2023.105455
Liu Y, Ji X, Nie X, Qu M, Zheng L, Tan Z, Zhao H, Huo L, Liu S, Zhang B, Wang Y (2015) Arabidopsis AtbHLH112 regulates the expression of genes involved in abiotic stress tolerance by binding to their E-box and GCG-box motifs. New Phytol 207(3):692–709. https://doi.org/10.1111/nph.13387
doi: 10.1111/nph.13387
pubmed: 25827016
Liu C, Mao B, Yuan D, Chu C, Duan M (2022) Salt tolerance in rice: physiological responses and molecular mechanisms. Crop J 10(1):13–25. https://doi.org/10.1016/j.cj.2021.02.010
doi: 10.1016/j.cj.2021.02.010
Lv X, Yu P, Deng W, Li Y (2018) Transcriptomic analysis reveals the molecular adaptation to NaCl stress in Zostera marina L. Plant Physiol Biochem 130:61–68. https://doi.org/10.1016/j.plaphy.2018.06.022
doi: 10.1016/j.plaphy.2018.06.022
pubmed: 29960892
Malakar P, Chattopadhyay D (2021) Adaptation of plants to salt stress: the role of the ion transporters. J Plant Biochem Biotechnol 30(4):668–683. https://doi.org/10.1007/s13562-021-00741-6
doi: 10.1007/s13562-021-00741-6
Marín-Guirao L, Sandoval-Gil JM, Bernardeau-Esteller J, Ruíz JM, Sánchez-Lizaso JL (2013) Responses of the Mediterranean seagrass Posidonia oceanica to hypersaline stress duration and recovery. Mar Environ Res 84:60–75. https://doi.org/10.1016/j.marenvres.2012.12.001
doi: 10.1016/j.marenvres.2012.12.001
pubmed: 23306019
Mekawy AMM, Assaha DVM, Yahagi H, Tada Y, Ueda A, Saneoka H (2015) Growth, physiological adaptation, and gene expression analysis of two Egyptian rice cultivars under salt stress. Plant Physiol Biochem 87:17–25. https://doi.org/10.1016/j.plaphy.2014.12.007
doi: 10.1016/j.plaphy.2014.12.007
pubmed: 25532120
Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7(9):405–410. https://doi.org/10.1016/s1360-1385(02)02312-9
doi: 10.1016/s1360-1385(02)02312-9
pubmed: 12234732
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681. https://doi.org/10.1146/annurev.arplant.59.032607.092911
doi: 10.1146/annurev.arplant.59.032607.092911
pubmed: 18444910
Munns R, James RA, Läuchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57(5):1025–1043. https://doi.org/10.1093/jxb/erj100
doi: 10.1093/jxb/erj100
pubmed: 16510517
Mutwakil MZ, Hajrah NH, Atef A, Edris S, Sabir MJ, Al-Ghamdi AK, Sabir MJSM, Nelson C, Makki RM, Ali HM, El-Domyati FM, Al-Hajar ASM, Gloaguen Y, Al-Zahrani HS, Sabir JSM, Jansen RK, Bahieldin A, Hall N (2017) Transcriptomic and metabolic responses of Calotropis procera to salt and drought stress. BMC Plant Biol 17(1):231. https://doi.org/10.1186/s12870-017-1155-7
doi: 10.1186/s12870-017-1155-7
pubmed: 29202709
pmcid: 5716246
Obata T, Kitamoto HK, Nakamura A, Fukuda A, Tanaka Y (2007) Rice shaker potassium channel OsKAT1 confers tolerance to salinity stress on yeast and rice cells. Plant Physiol 144(4):1978–1985. https://doi.org/10.1104/pp.107.101154
doi: 10.1104/pp.107.101154
pubmed: 17586689
pmcid: 1949902
Olsen JL, Rouzé P, Verhelst B, Lin Y-C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins JW, Jueterbock A, Mraz A, Stam WT, Tice H, Bornberg-Bauer E, Green PJ, Pearson GA, Procaccini G, Duarte CM, Schmutz J, Reusch TBH, Van de Peer Y (2016) The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature 530(7590):331–335. https://doi.org/10.1038/nature16548
doi: 10.1038/nature16548
pubmed: 26814964
Planchet E, Verdu I, Delahaie J, Cukier C, Girard C, Morère-Le Paven M-C, Limami AM (2014) Abscisic acid-induced nitric oxide and proline accumulation in independent pathways under water-deficit stress during seedling establishment in Medicago truncatula. J Exp Bot 65(8):2161–2170. https://doi.org/10.1093/jxb/eru088
doi: 10.1093/jxb/eru088
pubmed: 24604737
Pospíšil P (2009) Production of reactive oxygen species by photosystem II. Biochim Biophys Acta BBA-Bioenerg 1787(10):1151–1160. https://doi.org/10.1016/j.bbabio.2009.05.005
doi: 10.1016/j.bbabio.2009.05.005
Qian Y, Zhang T, Yu Y, Gou L, Yang J, Xu J, Pi E (2021) Regulatory mechanisms of bHLH transcription factors in plant adaptive responses to various abiotic stresses. Front Plant Sci. https://doi.org/10.3389/fpls.2021.677611
doi: 10.3389/fpls.2021.677611
pubmed: 35154201
pmcid: 8716879
Saddhe AA, Mishra AK, Kumar K (2021) Molecular insights into the role of plant transporters in salt stress response. Physiol Plant 173(4):1481–1494. https://doi.org/10.1111/ppl.13453
doi: 10.1111/ppl.13453
pubmed: 33963568
Sandoval-Gil JM, Ruiz JM, Marín-Guirao L (2023) Advances in understanding multilevel responses of seagrasses to hypersalinity. Mar Environ Res 183:105809. https://doi.org/10.1016/j.marenvres.2022.105809
doi: 10.1016/j.marenvres.2022.105809
pubmed: 36435174
Satoh K, Smith CM, Fork DC (1983) Effects of salinity on primary processes of photosynthesis in the Red Alga Porphyra perforata. Plant Physiol 73(3):643–647. https://doi.org/10.1104/pp.73.3.643
doi: 10.1104/pp.73.3.643
pubmed: 16663274
pmcid: 1066522
Shabala S, Cuin TA (2008) Potassium transport and plant salt tolerance. Physiol Plant 133(4):651–669. https://doi.org/10.1111/j.1399-3054.2007.01008.x
doi: 10.1111/j.1399-3054.2007.01008.x
pubmed: 18724408
Shafer DJ, Kaldy JE, Sherman TD, Marko KM (2011) Effects of salinity on photosynthesis and respiration of the seagrass Zostera japonica: A comparison of two established populations in North America. Aquat Bot 95(3):214–220. https://doi.org/10.1016/j.aquabot.2011.06.003
doi: 10.1016/j.aquabot.2011.06.003
Sharma A, Shahzad B, Rehman A, Bhardwaj R, Landi M, Zheng B (2019) Response of phenylpropanoid pathway and the role of polyphenols in plants under abiotic stress. Molecules 24(13):2452. https://doi.org/10.3390/molecules24132452
doi: 10.3390/molecules24132452
pubmed: 31277395
pmcid: 6651195
Tian Q, Shen L, Luan J, Zhou Z, Guo D, Shen Y, Jing W, Zhang B, Zhang Q, Zhang W (2021) Rice shaker potassium channel OsAKT2 positively regulates salt tolerance and grain yield by mediating K
doi: 10.1111/pce.14101
pubmed: 34008219
Tolleter D, Jaquinod M, Mangavel C, Passirani C, Saulnier P, Manon S, Teyssier E, Payet N, Avelange-Macherel M-H, Macherel D (2007) Structure and function of a mitochondrial late embryogenesis abundant protein are revealed by desiccation. Plant Cell 19(5):1580–1589. https://doi.org/10.1105/tpc.107.050104
doi: 10.1105/tpc.107.050104
pubmed: 17526751
pmcid: 1913742
Touchette BW (2007) Seagrass-salinity interactions: Physiological mechanisms used by submersed marine angiosperms for a life at sea. J Exp Mar Biol Ecol 350(1):194–215. https://doi.org/10.1016/j.jembe.2007.05.037
doi: 10.1016/j.jembe.2007.05.037
Tyerman SD, Hatcher AI, West RJ, Larkum AWD (1984) Posidonia australis growing in altered salinities: Leaf growth, regulation of turgor and the development of osmotic gradients. Aust J Plant Physiol 11:35–47
Vaahtera L, Schulz J, Hamann T (2019) Cell wall integrity maintenance during plant development and interaction with the environment. Nat Plants 5(9):924–932. https://doi.org/10.1038/s41477-019-0502-0
doi: 10.1038/s41477-019-0502-0
pubmed: 31506641
Van Diggelen J, Rozema J, Broekman R (1987) Mineral composition of and proline accumulation by zostera marina L. in response to environmental salinity. Aquat Bot 27(2):169–176. https://doi.org/10.1016/0304-3770(87)90064-7
doi: 10.1016/0304-3770(87)90064-7
van Zelm E, Zhang Y, Testerink C (2020) Salt tolerance mechanisms of plants. Annual Review Plant Biol 71(1):403–433. https://doi.org/10.1146/annurev-arplant-050718-100005
doi: 10.1146/annurev-arplant-050718-100005
Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu J-K (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J 45(4):523–539. https://doi.org/10.1111/j.1365-313X.2005.02593.x
doi: 10.1111/j.1365-313X.2005.02593.x
pubmed: 16441347
Wang C, Deng P, Chen L, Wang X, Ma H, Hu W, Yao N, Feng Y, Chai R, Yang G, He G (2013) A wheat WRKY transcription factor TaWRKY10 confers tolerance to multiple abiotic stresses in transgenic tobacco. PLoS ONE 8(6):e65120. https://doi.org/10.1371/journal.pone.0065120
doi: 10.1371/journal.pone.0065120
pubmed: 23762295
pmcid: 3677898
Wang F, Yang Y, Wang Z, Zhou J, Fan B, Chen Z (2015) A critical role of lyst-interacting protein5, a positive regulator of multivesicular body biogenesis, in plant responses to heat and salt stresses. Plant Physiol 169(1):497–511. https://doi.org/10.1104/pp.15.00518
doi: 10.1104/pp.15.00518
pubmed: 26229051
pmcid: 4577394
Wang L, Liu Y, Feng S, Wang Z, Zhang J, Zhang J, Wang D, Gan Y (2018) AtHKT1 gene regulating K
doi: 10.1038/s41598-018-34660-9
pubmed: 30410009
pmcid: 6224463
Wang G-L, Ren X-Q, Liu J-X, Yang F, Wang Y-P, Xiong A-S (2019) Transcript profiling reveals an important role of cell wall remodeling and hormone signaling under salt stress in garlic. Plant Physiol Biochem 135:87–98. https://doi.org/10.1016/j.plaphy.2018.11.033
doi: 10.1016/j.plaphy.2018.11.033
pubmed: 30529171
Wang H, Tang X, Chen J, Shang S, Zhu M, Liang S, Zang Y (2021) Comparative studies on the response of Zostera marina leaves and roots to ammonium stress and effects on nitrogen metabolism. Aquat Toxicol 240:105965. https://doi.org/10.1016/j.aquatox.2021.105965
doi: 10.1016/j.aquatox.2021.105965
pubmed: 34543784
Widodo PJH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and clipper, which differ in salinity tolerance. J Exp Bot 60(14):4089–4103. https://doi.org/10.1093/jxb/erp243
doi: 10.1093/jxb/erp243
pubmed: 19666960
pmcid: 2755029
Wu H, Zhang X, Giraldo JP, Shabala S (2018) It is not all about sodium: revealing tissue specificity and signalling roles of potassium in plant responses to salt stress. Plant Soil 431(1):1–17. https://doi.org/10.1007/s11104-018-3770-y
doi: 10.1007/s11104-018-3770-y
Yan H, Li Q, Park S-C, Wang X, Liu Y, Zhang Y, Tang W, Kou M, Ma D (2016) Overexpression of CuZnSOD and APX enhance salt stress tolerance in sweet potato. Plant Physiol Biochem 109:20–27. https://doi.org/10.1016/j.plaphy.2016.09.003
doi: 10.1016/j.plaphy.2016.09.003
pubmed: 27620271
Yan J, He H, Fang L, Zhang A (2018) Pectin methylesterase31 positively regulates salt stress tolerance in Arabidopsis. Biochem Biophys Res Commun 496(2):497–501. https://doi.org/10.1016/j.bbrc.2018.01.025
doi: 10.1016/j.bbrc.2018.01.025
pubmed: 29307824
Yang Y, Guo Y (2018) Elucidating the molecular mechanisms mediating plant salt-stress responses. New Phytol 217(2):523–539. https://doi.org/10.1111/nph.14920
doi: 10.1111/nph.14920
pubmed: 29205383
Yarra R (2019) The wheat NHX gene family: Potential role in improving salinity stress tolerance of plants. Plant Gene 18:100178. https://doi.org/10.1016/j.plgene.2019.100178
doi: 10.1016/j.plgene.2019.100178
Zeng Y, Li Q, Wang H, Zhang J, Du J, Feng H, Blumwald E, Yu L, Xu G (2018) Two NHX-type transporters from Helianthus tuberosus improve the tolerance of rice to salinity and nutrient deficiency stress. Plant Biotechnol J 16(1):310–321. https://doi.org/10.1111/pbi.12773
doi: 10.1111/pbi.12773
pubmed: 28627026
Zhang H-X, Blumwald E (2001) Transgenic salt-tolerant tomato plants accumulate salt in foliage but not in fruit. Nat Biotechnol 19(8):765–768. https://doi.org/10.1038/90824
doi: 10.1038/90824
pubmed: 11479571
Zhang M, Zhang S (2022) Mitogen-activated protein kinase cascades in plant signaling. J Integr Plant Biol 64(2):301–341. https://doi.org/10.1111/jipb.13215
doi: 10.1111/jipb.13215
pubmed: 34984829
Zhang S-S, Sun L, Dong X, Lu S-J, Tian W, Liu J-X (2016) Cellulose synthesis genes CESA6 and CSI1 are important for salt stress tolerance in Arabidopsis. J Integr Plant Biol 58(7):623–626. https://doi.org/10.1111/jipb.12442
doi: 10.1111/jipb.12442
pubmed: 26503768
Zhang B, Li P, Su T, Li P, Xin X, Wang W, Zhao X, Yu Y, Zhang D, Yu S, Zhang F (2020a) Comprehensive analysis of wall-associated kinase genes and their expression under abiotic and biotic stress in Chinese cabbage (Brassica rapa ssp. pekinensis). J Plant Growth Regul 39(1):72–86. https://doi.org/10.1007/s00344-019-09964-3
doi: 10.1007/s00344-019-09964-3
Zhang P, Wang R, Yang X, Ju Q, Li W, Lü S, Tran L-SP, Xu J (2020b) The R2R3-MYB transcription factor AtMYB49 modulates salt tolerance in Arabidopsis by modulating the cuticle formation and antioxidant defence. Plant Cell Environ 43(8):1925–1943. https://doi.org/10.1111/pce.13784
doi: 10.1111/pce.13784
pubmed: 32406163
Zhang Y, Zhao P, Yue S, Liu M, Qiao Y, Xu S, Gu R, Zhang X, Zhou Y (2021) New insights into physiological effects of anoxia under darkness on the iconic seagrass Zostera marina based on a combined analysis of transcriptomics and metabolomics. Sci Total Environ 768:144717. https://doi.org/10.1016/j.scitotenv.2020.144717
doi: 10.1016/j.scitotenv.2020.144717
pubmed: 33736305
Zhao C, Zhang H, Song C, Zhu J-K, Shabala S (2020) Mechanisms of plant responses and adaptation to soil salinity. Innov 1(1):100017. https://doi.org/10.1016/j.xinn.2020.100017
doi: 10.1016/j.xinn.2020.100017
Zhao S, Zhang Q, Liu M, Zhou H, Ma C, Wang P (2021) Regulation of plant responses to salt stress. Int J Mol Sci. https://doi.org/10.3390/ijms22094609
doi: 10.3390/ijms22094609
pubmed: 35008842
pmcid: 8745693
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
doi: 10.1146/annurev.arplant.53.091401.143329
pubmed: 12221975
pmcid: 3128348