Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (8): 2384-2396    DOI: 10.1016/j.jia.2023.07.015
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
SlTPP4 participates in ABA-mediated salt tolerance by enhancing root architecture in tomato

DU Dan1*, HU Xin1*, SONG Xiao-mei1, XIA Xiao-jiao1, SUN Zhen-yu1, LANG Min1, PAN Yang-lu1, ZHENG Yu1, 2#, PAN Yu1#

1 Key Laboratory of Horticulture Science for Southern Mountainous Regions, Ministry of Education/College of Horticulture and Landscape Architecture/Academy of Agricultural Sciences, Southwest University, Chongqing 400715, P.R.China

2 Chongqing Vocational Institute of Engineering, Chongqing 402260, P.R.China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      



Salinity tolerance is an important physiological index for crop breeding.  Roots are typically the first plant tissue to withstand salt stress.  In this study, we found that the tomato (Solanum lycopersicum) trehalose-6-phosphate phosphatase (SlTPP4) gene is induced by abscisic acid (ABA) and salt, and is mainly expressed in roots.  Overexpression of SlTPP4 in tomato enhanced tolerance to salt stress, resulting in better growth performance.  Under saline conditions, SlTPP4 overexpression plants demonstrated enhanced sucrose metabolism, as well as increased expression of genes related to salt tolerance.  At the same time, expression of genes related to ABA biosynthesis and signal transduction was enhanced or altered, respectively.  In-depth exploration demonstrated that SlTPP4 enhances Casparian band development in roots to restrict the intake of Na+.  Our study thus clarifies the mechanism of SlTPP4-mediated salt tolerance, which will be of great importance for the breeding of salt-tolerant tomato crops.

Keywords:  trehalose-6-phosphate phosphatase (TPP)        salt tolerance        root        ABA        tomato (Solanum lycopersicum)  
Received: 21 December 2022   Accepted: 26 June 2023

This work was supported by the National Natural Science Foundation of China (32172597), the Chongqing Post Doctoral Special Support Project, China (2112012724652268), the Chongqing Exceptional Young Talents Project, China (CQYC202005097) and the Chongqing Natural Science Foundation, China (cstc2018jcyjAX0730).

About author:  #Correspondence ZHENG Yu, Tel: +86-23-61065440, E-mail:; PAN Yu, Tel: +86-23-68250227, E-mail: * These authors contributed equally to this study.

Cite this article: 

DU Dan, HU Xin, SONG Xiao-mei, XIA Xiao-jiao, SUN Zhen-yu, LANG Min, PAN Yang-lu, ZHENG Yu, PAN Yu. 2023. SlTPP4 participates in ABA-mediated salt tolerance by enhancing root architecture in tomato. Journal of Integrative Agriculture, 22(8): 2384-2396.

Alla M M N, Badran E G, Mohammed F A. 2018. Exogenous trehalose alleviates the adverse effects of NaCl stress in wheat. Agrochimica62, 127–142.

Baena-Gonzalez E, Rolland F, Thevelein J M, Sheen J. 2007. A central integrator of transcription networks in plant stress and energy signalling. Nature448, 938–942.

Belda-Palazon B, Adamo M, Valerio C, Ferreira L J, Confraria A, Reis-Barata D, Rodrigues A, Meyer C, Rodriguez P L, Baena-Gonzalez E. 2020. A dual function of SnRK2 kinases in the regulation of SnRK1 and plant growth. Nature Plants6, 1345–1353.

Belda-Palazon B, Costa M, Beeckman T, Rolland F, Baena-Gonzalez E. 2022. ABA represses TOR and root meristem activity through nuclear exit of the SnRK1 kinase. Proceedings of the National Academy of Sciences of the United States of America119, e2204862119.

Bose J, Rodrigo-Moreno A, Lai D W, Xie Y J, Shen W B, Shabala S. 2015. Rapid regulation of the plasma membrane H+-ATPase activity is essential to salinity tolerance in two halophyte species, Atriplex lentiformis and Chenopodium quinoaAnnals of Botany115, 481–494.

Brodmann D, Schuller A, Ludwig-Muller J, Aeschbacher R A, Wiemken A, Boller T, Wingler A. 2002. Induction of trehalase in Arabidopsis plants infected with the trehalose-producing pathogen Plasmodiophora brassicaeMolecular Plant–Microbe Interactions15, 693–700.

Devkar V, Thirumalaikumar V P, Xue G P, Vallarino J G, Tureckova V, Strnad M, Fernie A R, Hoefgen R, Mueller-Roeber B, Balazadeh S. 2020. Multifaceted regulatory function of tomato SlTAF1 in the response to salinity stress. New Phytologist225, 1681–1698.

Fernandez O, Bethencourt L, Quero A, Sangwan R S, Clement C. 2010. Trehalose and plant stress responses: Friend or foe? Trends in Plant Science15, 409–417.

Fichtner F, Barbier F F, Annunziata M G, Feil R, Olas J J, Mueller-Roeber B, Stitt M, Beveridge C A, Lunn J E. 2021. Regulation of shoot branching in arabidopsis by trehalose 6-phosphate. New Phytologist229, 2135–2151.

Fu Y Y, Zhang Z H, Liu J, Chen M, Pan R H, Hu W M, Guan Y J, Hu J. 2020. Seed priming with spermidine and trehalose enhances chilling tolerance of rice via different mechanisms. Journal of Plant Growth Regulation39, 669–679.

Geng Y, Wu R, Wee C W, Xie F, Wei X, Chan P M, Tham C, Duan L, Dinneny J R. 2013. A spatio–temporal understanding of growth regulation during the salt stress response in ArabidopsisPlant Cell25, 2132–2154.

Goddijn O J M, Verwoerd T C, Voogd E, Krutwagen R, Degraaf P, Vandun K, Delaat A, Vandenelzen P, Damm B, Pen J. 1995. Transgenic tobacco plants as a model-system for the production of trehalose. Plant Physiology108, 149.

Halfter U, Ishitani M, Zhu J K. 2000. The Arabidopsis SOS2 protein kinase physically interacts with and is activated by the calcium-binding protein SOS3. Proceedings of the National Academy of Sciences of the United States of America97, 3735–3740.

Han C, Qiao Y, Yao L M, Hao W, Liu Y, Shi W, Fan M, Bai M Y. 2022. TOR and SnRK1 fine tune SPEECHLESS transcription and protein stability to optimize stomatal development in response to exogenously supplied sugar. New Phytologist234, 107–121.

Henry C, Bledsoe S W, Griffiths C A, Kollman A, Paul M J, Sakr S, Lagrimini L M. 2015. Differential role for trehalose metabolism in salt-stressed maize. Plant Physiology169, 1072–1089.

Jossier M, Bouly J P, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M. 2009. SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thalianaPlant Journal59, 316–328.

Jun S S, Yang J Y, Choi H Y, Kim N R, Park M C, Hong Y N. 2005. Altered physiology in trehalose-producing transgenic tobacco plants: Enhanced tolerance to drought and salinity stresses. Journal of Plant Biology48, 456–466.

Kim W Y, Ali Z, Park H J, Park S J, Cha J Y, Perez-Hormaeche J, Quintero F J, Shin G, Kim M R, Qiang Z, Ning L, Park H C, Lee S Y, Bressan R A, Pardo J M, Bohnert H J, Yun D J. 2013. Release of SOS2 kinase from sequestration with GIGANTEA determines salt tolerance in ArabidopsisNature Communications4, 1352.

Lin H X, Yang Y Q, Quan R D, Mendoza I, Wu Y S, Du W M, Zhao S S, Schumaker K S, Pardo J M, Guo Y. 2009. Phosphorylation of SOS3-LIKE CALCIUM BINDING PROTEIN8 by SOS2 protein kinase stabilizes their protein complex and regulates salt tolerance in ArabidopsisPlant Cell21, 1607–1619.

Lin Q F, Wang S, Dao Y H, Wang J Y, Wang K. 2020. Arabidopsis thaliana trehalose-6-phosphate phosphatase gene TPPI enhances drought tolerance by regulating stomatal apertures. Journal of Experimental Botany71, 4285–4297.

Lin Q F, Yang J, Wang Q L, Zhu H, Chen Z Y, Dao Y H, Wang K. 2019. Overexpression of the trehalose-6-phosphate phosphatase family gene AtTPPF improves the drought tolerance of Arabidopsis thalianaBMC Plant Biology19, 381.

Liu H, Yu C Y, Li H X, Ouyang B, Wang T T, Zhang J H, Wang X, Ye Z B. 2015. Overexpression of ShDHN, a dehydrin gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses in tomato. Plant Science231, 198–211.

Lyu J I, Park J H, Kim J K, Bae C H, Jeong W J, Min S R, Liu J R. 2018. Enhanced tolerance to heat stress in transgenic tomato seeds and seedlings overexpressing a trehalose-6-phosphate synthase/phosphatase fusion gene. Plant Biotechnology Reports12, 399–408.

Ma L, Liu X H, Lv W J, Yang Y Q. 2022. Molecular mechanisms of plant responses to salt stress. Frontiers in Plant Science13, 934877.

McLoughlin F, Galvan-Ampudia C S, Julkowska M M, Caarls L, van der Does D, Lauriere C, Munnik T, Haring M A, Testerink C. 2012. The Snf1-related protein kinases SnRK2.4 and SnRK2.10 are involved in maintenance of root system architecture during salt stress. Plant Journal72, 436–449.

Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Annual Review of Plant Biology59, 651–681.

Nuccio M L, Wu J, Mowers R, Zhou H P, Meghji M, Primavesi L F, Paul M J, Chen X, Gao Y, Haque E, Basu S S, Lagrimini L M. 2015. Expression of trehalose-6-phosphate phosphatase in maize ears improves yield in well-watered and drought conditions. Nature Biotechnology33, 862–869.

Park S Y, Fung P, Nishimura N, Jensen D R, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T F F, Alfred S E, Bonetta D, Finkelstein R, Provart N J, Desveaux D, Rodriguez P L, McCourt P, Zhu J K, Schroeder J I, Volkman B F, et al. 2009. Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of START proteins. Science324, 1068–1071.

Peixoto B, Baena-Gonzalez E. 2022. Management of plant central metabolism by SnRK1 protein kinases. Journal of Experimental Botany, 73, 7068–7082.

Ponnu J, Schlereth A, Zacharaki V, Dzialo M A, Abel C, Feil R, Schmid M, Wahl V. 2020. The trehalose 6-phosphate pathway impacts vegetative phase change in Arabidopsis thalianaPlant Journal104, 768–780.

Quintero F J, Martinez-Atienza J, Villalta I, Jiang X Y, Kim W Y, Ali Z, Fujii H, Mendoza I, Yun D J, Zhu J K, Pardo J M. 2011. Activation of the plasma membrane Na/H antiporter Salt-Overly-Sensitive 1 (SOS1) by phosphorylation of an auto-inhibitory C-terminal domain. Proceedings of the National Academy of Sciences of the United States of America108, 2611–2616.

Rahman M M, Rahman M M, Eom J S, Jeon J S. 2021. Genome-wide identification, expression profiling and promoter analysis of trehalose-6-phosphate phosphatase gene family in rice. Journal of Plant Biology64, 55–71.

Redillas M C F R, Park S H, Lee J W, Kim Y S, Jeong J S, Jung H, Bang S W, Hahn T R, Kim J K. 2012. Accumulation of trehalose increases soluble sugar contents in rice plants conferring tolerance to drought and salt stress. Plant Biotechnology Reports6, 89–96.

Reignault P, Cogan A, Muchembled J, Sahraoui A L H, Durand R, Sancholle M. 2001. Trehalose induces resistance to powdery mildew in wheat. New Phytologist149, 519–529.

Roy S J, Negrao S, Tester M. 2014. Salt resistant crop plants. Current Opinion in Biotechnology26, 115–124.

Satoh-Nagasawa N, Nagasawa N, Malcomber S, Sakai H, Jackson D. 2006. A trehalose metabolic enzyme controls inflorescence architecture in maize. Nature441, 227–230.

Shabala S. 2013. Learning from halophytes: Physiological basis and strategies to improve abiotic stress tolerance in crops. Annals of Botany112, 1209–1221.

Vandesteene L, Lopez-Galvis L, Vanneste K, Feil R, Maere S, Lammens W, Rolland F, Lunn J E, Avonce N, Beeckman T, Van Dijck P. 2012. Expansive evolution of the TREHALOSE-6-PHOSPHATE PHOSPHATASE gene family in Arabidopsis. Plant Physiology160, 884–896.

Vishal B, Krishnamurthy P, Ramamoorthy R, Kumar P P. 2019. OsTPS8 controls yield-related traits and confers salt stress tolerance in rice by enhancing suberin deposition. New Phytologist221, 1369–1386.

Yang Z J, Wang C W, Xue Y, Liu X, Chen S, Song C P, Yang Y Q, Guo Y. 2019. Calcium-activated 14-3-3 proteins as a molecular switch in salt stress tolerance. Nature Communications10, 1199.

Yu W Q, Zhao R R, Wang L, Zhang S J, Li R, Sheng J P, Shen L. 2019. ABA signaling rather than ABA metabolism is involved in trehalose-induced drought tolerance in tomato plants. Planta250, 643–655.

Yuan F, Yang H M, Xue Y, Kong D D, Ye R, Li C J, Zhang J Y, Theprungsirikul L, Shrift T, Krichilsky B, Johnson D M, Swift G B, He Y K, Siedow J N, Pei Z M. 2015. OSCA1 mediates osmotic-stress-evoked Ca2+ increases vital for osmosensing in ArabidopsisNature514, 367–371.

Zhang H J, Hong Y B, Huang L, Liu S X, Tian L M, Dai Y, Cao Z Y, Huang L H, Li D Y, Song F M. 2016. Virus-induced gene silencing-based functional analyses revealed the involvement of several putative trehalose-6-phosphate synthase/phosphatase genes in disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 in tomato. Frontiers in Plant Science7, 1176.

Zhang H J, Mao L L, Xin M, Xing H X, Zhang Y A, Wu J, Xu D L, Wang Y M, Shang Y Q, Wei L M, Cui M S, Zhuang T, Sun X Z, Song X L. 2022. Overexpression of GhABF3 increases cotton (Gossypium hirsutum L.) tolerance to salt and drought. BMC Plant Biology22, 313.

Zhang L A, Wang L T, Chen X, Zhao L J, Liu X Y, Wang Y H, Wu G F, Xia C, Zhang L C, Kong X Y. 2022. The protein phosphatase 2C clade A TaPP2CA interact with calcium-dependent protein kinases, TaCDPK5/TaCDPK9-1, that phosphorylate TabZIP60 transcription factor from wheat (Triticum aestivum L.). Plant Science321, 111304.

Zhao C, Zhang H, Song C, Zhu J K, Shabala S. 2020. Mechanisms of plant responses and adaptation to soil salinity. The Innovation1, 100017.

Zhou H P, Lin H X, Chen S, Becker K, Yang Y Q, Zhao J F, Kudla J, Schumaker K S, Guo Y. 2014. Inhibition of the Arabidopsis salt overly sensitive pathway by 14-3-3 proteins. Plant Cell26, 1166–1182.

No related articles found!
No Suggested Reading articles found!