Genome-Wide Analysis of Trehalose-6-Phosphate Phosphatase Gene Family and Their Expression Profiles in Response to Abiotic Stress in Groundnut

Overview

Journal Plants (Basel)

Date 2024 Apr 27

PMID 38674465

Authors

Yue Liu

Xin Wang

Lei Ouyang

Ruonan Yao

Zhihui Wang

Yanping Kang

Liying Yan

Yuning Chen

Dongxin Huai

Qianqian Wang

Huifang Jiang

Yong Lei

Boshou Liao

Affiliations

Soon will be listed here.

Abstract

Trehalose-6-phosphate phosphatase (TPP) is a pivotal enzyme in trehalose biosynthesis which plays an essential role in plant development and in the abiotic stress response. However, little is currently known about in groundnut. In the present study, a total of 16 genes were identified, and can be divided into three phylogenetic subgroups. AhTPP members within the same subgroups generally displayed similar exon-intron structures and conserved motifs. Gene collinearity analysis revealed that segmental duplication was the primary factor driving the expansion of the family. An analysis of the upstream promoter region of revealed eight hormone- and four stress-related responsive -elements. Transcriptomic analysis indicated high expression levels of genes in roots or flowers, while RT-qPCR analysis showed upregulation of the six tested genes under different abiotic stresses, suggesting that play roles in growth, development, and response to various abiotic stresses. Subcellular localization analysis showed that AhTPP1A and AhTPP5A were likely located in both the cytoplasm and the nucleus. To further confirm their functions, the genes and were individually integrated into yeast expression vectors. Subsequent experiments demonstrated that yeast cells overexpressing these genes displayed increased tolerance to osmotic and salt stress compared to the control group. This study will not only lay the foundation for further study of gene functions, but will also provide valuable gene resources for improving abiotic stress tolerance in groundnut and other crops.

References

Ponnu J, Wahl V, Schmid M . Trehalose-6-phosphate: connecting plant metabolism and development. Front Plant Sci. 2012; 2:70. PMC: 3355582. DOI: 10.3389/fpls.2011.00070. View

Figueroa C, Lunn J . A Tale of Two Sugars: Trehalose 6-Phosphate and Sucrose. Plant Physiol. 2016; 172(1):7-27. PMC: 5074632. DOI: 10.1104/pp.16.00417. View

Ouyang L, Liu Y, Yao R, He D, Yan L, Chen Y . Genome-wide analysis of UDP-glycosyltransferase gene family and identification of a flavonoid 7-O-UGT (AhUGT75A) enhancing abiotic stress in peanut (Arachis hypogaea L.). BMC Plant Biol. 2023; 23(1):626. PMC: 10702079. DOI: 10.1186/s12870-023-04656-3. View

Du L, Li S, Ding L, Cheng X, Kang Z, Mao H . Genome-wide analysis of trehalose-6-phosphate phosphatases (TPP) gene family in wheat indicates their roles in plant development and stress response. BMC Plant Biol. 2022; 22(1):120. PMC: 8925099. DOI: 10.1186/s12870-022-03504-0. View

Guo A, Zhu Q, Chen X, Luo J . [GSDS: a gene structure display server]. Yi Chuan. 2007; 29(8):1023-6. View

Lin Q, Wang S, Dao Y, Wang J, Wang K . Arabidopsis thaliana trehalose-6-phosphate phosphatase gene TPPI enhances drought tolerance by regulating stomatal apertures. J Exp Bot. 2020; 71(14):4285-4297. DOI: 10.1093/jxb/eraa173. View

Ge L, Chao D, Shi M, Zhu M, Gao J, Lin H . Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta. 2008; 228(1):191-201. DOI: 10.1007/s00425-008-0729-x. View

Shao W, Zhang X, Zhou Z, Ma Y, Chu D, Wang L . Genome- and transcriptome-wide identification of trehalose-6-phosphate phosphatases (TPP) gene family and their expression patterns under abiotic stress and exogenous trehalose in soybean. BMC Plant Biol. 2023; 23(1):641. PMC: 10714469. DOI: 10.1186/s12870-023-04652-7. View

Joshi R, Sahoo K, Singh A, Anwar K, Pundir P, Gautam R . Enhancing trehalose biosynthesis improves yield potential in marker-free transgenic rice under drought, saline, and sodic conditions. J Exp Bot. 2019; 71(2):653-668. PMC: 6946002. DOI: 10.1093/jxb/erz462. View

10.

Henry C, Bledsoe S, Griffiths C, Kollman A, Paul M, Sakr S . Differential Role for Trehalose Metabolism in Salt-Stressed Maize. Plant Physiol. 2015; 169(2):1072-89. PMC: 4587459. DOI: 10.1104/pp.15.00729. View

11.

Voorrips R . MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered. 2002; 93(1):77-8. DOI: 10.1093/jhered/93.1.77. View

12.

Carillo P, Feil R, Gibon Y, Satoh-Nagasawa N, Jackson D, Blasing O . A fluorometric assay for trehalose in the picomole range. Plant Methods. 2013; 9(1):21. PMC: 3698175. DOI: 10.1186/1746-4811-9-21. View

13.

Kerbler S, Armijos-Jaramillo V, Lunn J, Vicente R . The trehalose 6-phosphate phosphatase family in plants. Physiol Plant. 2023; 175(6):e14096. DOI: 10.1111/ppl.14096. View

14.

Avonce N, Mendoza-Vargas A, Morett E, Iturriaga G . Insights on the evolution of trehalose biosynthesis. BMC Evol Biol. 2006; 6:109. PMC: 1769515. DOI: 10.1186/1471-2148-6-109. View

15.

Vandesteene L, Lopez-Galvis L, Vanneste K, Feil R, Maere S, Lammens W . Expansive evolution of the trehalose-6-phosphate phosphatase gene family in Arabidopsis. Plant Physiol. 2012; 160(2):884-96. PMC: 3461562. DOI: 10.1104/pp.112.201400. View

16.

Lunn J . Gene families and evolution of trehalose metabolism in plants. Funct Plant Biol. 2020; 34(6):550-563. DOI: 10.1071/FP06315. View

17.

Clevenger J, Chu Y, Scheffler B, Ozias-Akins P . A Developmental Transcriptome Map for Allotetraploid . Front Plant Sci. 2016; 7:1446. PMC: 5043296. DOI: 10.3389/fpls.2016.01446. View

18.

Wang D, Zhang Y, Zhang Z, Zhu J, Yu J . KaKs_Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics. 2010; 8(1):77-80. PMC: 5054116. DOI: 10.1016/S1672-0229(10)60008-3. View

19.

Krasensky J, Broyart C, Rabanal F, Jonak C . The redox-sensitive chloroplast trehalose-6-phosphate phosphatase AtTPPD regulates salt stress tolerance. Antioxid Redox Signal. 2014; 21(9):1289-304. PMC: 4158992. DOI: 10.1089/ars.2013.5693. View

20.

Wang Y, Tang H, DeBarry J, Tan X, Li J, Wang X . MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res. 2012; 40(7):e49. PMC: 3326336. DOI: 10.1093/nar/gkr1293. View