Comparative transcriptome analysis reveals gene network regulation of TGase-induced thermotolerance in tomato

Authors

  • Mohammad S. JAHAN Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095; Sher-e-Bangla Agricultural University, Faculty of Agriculture, Department of Horticulture, Dhaka 1207 (BD)
  • Zhengrong SHI Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095 (CN)
  • Min ZHONG Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095 (CN)
  • Yuemei ZHANG Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095 (CN)
  • Ranran ZHOU Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095 (CN)
  • Mohamed M. EL-MOGY Cairo University, Faculty of Agriculture, Vegetable Crop Department, 12613 Giza (EG)
  • Jin SUN Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095; Nanjing Agricultural University, Suqian Academy of Protected Horticulture, Suqian 223800 (CN)
  • Sheng SHU Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095; Nanjing Agricultural University, Suqian Academy of Protected Horticulture, Suqian 223800 (CN)
  • Shirong GUO Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095; Nanjing Agricultural University, Suqian Academy of Protected Horticulture, Suqian 223800 (CN)
  • Yu WANG Nanjing Agricultural University, College of Horticulture, Key Laboratory of Southern Vegetable Crop Genetic Improvement in Ministry of Agriculture, Nanjing 210095 (CN)

DOI:

https://doi.org/10.15835/nbha49112208

Keywords:

high temperature; photosynthesis; tomato; transglutaminase; transcriptome

Abstract

Transglutaminase (TGase), the ubiquitous protein in plants, catalyzes the post-translational transformation of proteins and plays a vital role in photosynthesis. However, its role and mechanism in tomato subjected to heat stress still remain unknown. Here, we carried out a transcriptomic assay to compare the differentially expressed genes (DEGs) between wild type (WT) and TGase overexpression (TGaseOE) plants employed to high-temperature at 42 °C and samples were collected after 0, 6, and 12 h, respectively. A total of 11,516 DEGs were identified from heat-stressed seedlings, while 1,148 and 1,353 DEGs were up-and down-regulated, respectively. The DEGs upon high-temperature stress were closely associated with the pathways encompassing protein processing in the endoplasmic reticulum, carbon fixation, and photosynthetic metabolism. In addition, 425 putative transcription factors (TFs) were identified, and the majority of them associated with the bHLH, HSF, AP2/ERF, MYB, and WRKY families. RNA-seq data validation further confirmed that 8 genes were linked to protein processing and photosynthesis, and the mRNA level of these genes in TGaseOE was higher than that in WT plants, which is consistent in transcriptome results. In conclusion, these results reveal the transcriptional regulation between WT and TGaseOE in tomato under heat stress and shed light on a new dimension of knowledge of TGase-mediated thermotolerance mechanism at the molecular level.

References

Aloisi I, Cai G, Serafini-Fracassini D, Del Duca S (2016). Transglutaminase as polyamine mediator in plant growth and differentiation. Amino Acids 48(10):2467-2478. https://doi.org/10.1007/s00726-016-2235-y

Bita CE, Gerats T (2013). Plant tolerance to high temperature in a changing environment: scientific fundamentals and production of heat stress-tolerant crops. Frontiers in Plant Science 4:273. https://doi.org/10.3389/fpls.2013.00273

Campos A, Carvajal-Vallejos PK, Villalobos E, Franco CF, Almeida AM, Coelho AV, Torne JM, Santos M (2010). Characterisation of Zea mays L. plastidial transglutaminase: interactions with thylakoid membrane proteins. Plant Biology 12(5):708-716. https://doi.org/10.1111/j.1438-8677.2009.00280.x

Campos N, Castanon S, Urreta I, Santos M, Torne JM (2013). Rice transglutaminase gene: identification, protein expression, functionality, light dependence and specific cell location. Plant Science 205:97-110. https://doi.org/10.1016/j.plantsci.2013.01.014

Castelan-Munoz N, Herrera J, Cajero-Sanchez W, Arrizubieta M, Trejo C, Garcia-Ponce B, ... Garay-Arroyo A (2019). MADS-Box genes are key components of genetic regulatory networks involved in abiotic stress and plastic developmental responses in plants. Frontiers in Plant Science 10:853. https://doi.org/10.3389/fpls.2019.00853

Chang L, Guo A, Jin X, Yang Q, Wang D, Sun Y, … Wang X (2015). The beta subunit of glyceraldehyde 3-phosphate dehydrogenase is an important factor for maintaining photosynthesis and plant development under salt stress-based on an integrative analysis of the structural, physiological and proteomic changes in chloroplasts in Thellungiella halophila. Plant Science 236:223-238. https://doi.org/10.1016/j.plantsci.2015.04.010

Del Duca S, Aloisi I, Parrotta L, Cai G (2019). Cytoskeleton, transglutaminase and gametophytic self-incompatibility in the Malinae (Rosaceae). International Journal of Molecular Sciences 20:209. https://doi.org/10.3390/ijms20010209

Del Duca S, Faleri C, Iorio RA, Cresti M, Serafini-Fracassini D, Cai G (2013). Distribution of transglutaminase in pear pollen tubes in relation to cytoskeleton and membrane dynamics. Plant Physiology 161(4):1706-1721. doi:10.1104/pp.112.212225

Della Mea M, Caparros-Ruiz D, Claparols I, Serafini-Fracassini D, Rigau J (2004). AtPng1p. The first plant transglutaminase. Plant Physiology 135(4):2046-2054. https://doi.org/10.1104/pp.104.042549

Du XP, Li WY, Sheng LP, Deng Y, Wang YJ, Zhang WW, … Chen SM (2018). Over-expression of chrysanthemum CmDREB6 enhanced tolerance of chrysanthemum to heat stress. BMC Plant Biology 18:178. https://doi.org/10.1186/s12870-018-1400-8

Engelken J, Funk C, Adamska I (2012). The extended light-harvesting complex (LHC) protein superfamily: classification and evolutionary dynamics. In: Burnap RL, Vermaas WFJ (Eds). Functional Genomics and Evolution of Photosynthetic Systems, pp 265-284. https://doi.org/10.1007/978-94-007-1533-2_11

Frank G, Pressman E, Ophir R, Althan L, Shaked R, Freedman M, Shen S, Firon N (2009). Transcriptional profiling of maturing tomato (Solanum lycopersicum L.) microspores reveals the involvement of heat shock proteins, ROS scavengers, hormones, and sugars in the heat stress response. Journal of Experimental Botany 60(13):3891-3908. https://doi.org/10.1093/jxb/erp234

Guo M, Liu JH, Ma X, Luo DX, Gong ZH, Lu MH (2016). The plant heat stress transcription factors (HSFs): structure, regulation, and function in response to abiotic stresses. Frontiers in Plant Science 7:114. https://doi.org/10.3389/fpls.2016.00114

Hong SW, Lee U, Vierling E (2003). Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiology 132(2):757-767. https://doi.org/10.1104/pp.102.017145

Ioannidis NE, Malliarakis D, Torne JM, Santos M, Kotzabasis K (2016). The over-expression of the plastidial transglutaminase from maize in Arabidopsis increases the activation threshold of photoprotection. Frontiers in Plant Science 7:635. https://doi.org/10.3389/fpls.2016.00635

Izumi M (2019). Heat shock proteins support refolding and shredding of misfolded proteins. Plant Physiology 180(4):1777-1778. https://doi.org/10.1104/pp.19.00711

Jahan MS, Guo S, Baloch AR, Sun J, Shu S, Wang Y, … Roy R (2020). Melatonin alleviates nickel phytotoxicity by improving photosynthesis, secondary metabolism and oxidative stress tolerance in tomato seedlings. Ecotoxicology and Environmental Safety 197:110593. https://doi.org/10.1016/j.ecoenv.2020.110593

Jahan MS, Shu S, Wang Y, Chen Z, He M, Tao M, … Guo S (2019a). Melatonin alleviates heat-induced damage of tomato seedlings by balancing redox homeostasis and modulating polyamine and nitric oxide biosynthesis. BMC Plant Biology 19:414. https://doi.org/10.1186/s12870-019-1992-7

Jahan MS, Wang Y, Shu S, Zhong M, Chen Z, Wu J, Sun J, Guo S (2019b). Exogenous salicylic acid increases the heat tolerance in tomato (Solanum lycopersicum L) by enhancing photosynthesis efficiency and improving antioxidant defense system through scavenging of reactive oxygen species. Scientia Horticulturae 247:421-429. https://doi.org/10.1016/j.scienta.2018.12.047

Katano K, Honda K, Suzuki N (2018). Integration between ROS regulatory systems and other signals in the regulation of various types of heat responses in plants. International Journal of Molecular Sciences 19:3370. https://doi.org/10.3390/ijms19113370

Kim YU, Lee BW (2019). Differential mechanisms of potato yield loss induced by high day and night temperatures during tuber initiation and bulking: photosynthesis and tuber growth. Frontiers in Plant Science 10:300. https://doi.org/10.3389/fpls.2019.00300

Klay I, Gouia S, Lu M, Mila I, Khoudi H, Bernadac A, Bouzayen M, Pirrello J (2018). Ethylene response factors (ERF) are differentially regulated by different abiotic stress types in tomato plants. Plant Science 274:137-145. https://doi.org/10.1016/j.plantsci.2018.05.023

Langmead B, Salzberg SL (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods 9(4):357-359. https://doi.org/10.1038/nmeth.1923

Li B, Gao K, Ren H, Tang W (2018). Molecular mechanisms governing plant responses to high temperatures. Journal of Integrative Plant Biology 60(9):757-779. https://doi.org/10.1111/jipb.12701

Li T, Xu X, Li Y, Wang H, Li Z, Li Z (2015). Comparative transcriptome analysis reveals differential transcription in heat-susceptible and heat-tolerant pepper (Capsicum annum L.) cultivars under heat stress. Journal of Plant Biology 58(6):411-424. https://doi.org/10.1007/s12374-015-0423-z

Li X, Wei W, Li F, Zhang L, Deng X, Liu Y, Yang S (2019). The plastidial glyceraldehyde-3-phosphate dehydrogenase is critical for abiotic stress response in wheat. International Journal of Molecular Sciences 20:1104. https://doi.org/10.3390/ijms20051104

Liu GT, Wang JF, Cramer G, Dai ZW, Duan W, Xu HG, … Li SH (2012). Transcriptomic analysis of grape (Vitis vinifera L.) leaves during and after recovery from heat stress. BMC Plant Biology 12:174.

https://doi.org/10.1186/1471-2229-12-174

Liu Y, Li J, Zhu Y, Jones A, Rose RJ, Song Y (2019). Heat stress in legume seed setting: effects, causes, and future prospects. Frontiers in Plant Science 10:938. https://doi.org/10.3389/fpls.2019.00938

Livak KJ, Schmittgen TD (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2-△△CT method. Methods 25(4):402-408. https://doi.org/10.1006/meth.2001.1262

Mandrone M, Antognoni F, Aloisi I, Potente G, Poli F, Cai G, ... Del Duca S (2019). Compatible and incompatible pollen-styles interaction in Pyrus communis L. show different transglutaminase features, polyamine pattern and metabolomics profiles. Frontiers in Plant Science 10:741. https://doi.org/10.3389/fpls.2019.00741

McLoughlin F, Kim M, Marshall RS, Vierstra RD, Vierling E (2019). HSP101 interacts with the proteasome and promotes the clearance of ubiquitylated protein aggregates. Plant Physiology 180(4):1829-1847. https://doi.org/10.1104/pp.19.00263

Ohama N, Sato H, Shinozaki K, Yamaguchi-Shinozaki K (2017). Transcriptional regulatory network of plant heat stress response. Trends in Plant Science 22(1):53-65. https://doi.org/10.1016/j.tplants.2016.08.015

Ortiz R, Braun HJ, Crossa J, Crouch JH, Davenport G, Dixon J, … Iwanaga M (2008). Wheat genetic resources enhancement by the international maize and wheat improvement center (CIMMYT). Genetic Resources and Crop Evolution 55:1095-1140. https://doi.org/10.1007/s10722-008-9372-4

Qian Y, Ren Q, Zhang J, Chen L (2019). Transcriptomic analysis of the maize (Zea mays L.) inbred line B73 response to heat stress at the seedling stage. Gene 692:68-78. https://doi.org/10.1016/j.gene.2018.12.062

Serafini-Fracassini D, Della Mea M, Tasco G, Casadio R, Del Duca S (2009). Plant and animal transglutaminases: do similar functions imply similar structures? Amino Acids 36(4):643-657.

https://doi.org/10.1007/s00726-008-0131-9

Silva J, Kim YJ, Sukweenadhi J, Rahimi S, Kwon WS, Yang DC (2016). Molecular characterization of 5-chlorophyll a/b-binding protein genes from Panax ginseng Meyer and their expression analysis during abiotic stresses. Photosynthetica 54(3):446-458. https://doi.org/10.1007/s11099-016-0189-7

Sung DY, Guy CL (2003). Physiological and molecular assessment of altered expression of Hsc70-1 in Arabidopsis. Evidence for pleiotropic consequences. Plant Physiology 132(2):979-987. https://doi.org/10.1104/pp.102.019398

Tang YY, Yuan YH, Shu S, Guo SR (2018). Regulatory mechanism of NaCl stress on photosynthesis and antioxidant capacity mediated by transglutaminase in cucumber (Cucumis sativus L.) seedlings. Scientia Horticulturae 235:294-306. https://doi.org/10.1016/j.scienta.2018.02.045

Tao MQ, Jahan MS, Hou K, Shu S, Wang Y, Sun J, Guo SR (2020). Bitter melon (Momordica charantia L.) rootstock improves the heat tolerance of cucumber by regulating photosynthetic and antioxidant defense pathways. Plants 9:692. https://doi.org/10.3390/plants9060692

Thirugnanasambantham K, Durairaj S, Saravanan S, Karikalan K, Muralidaran S, Islam VIH (2015). Role of ethylene response transcription factor (ERF) and its regulation in response to stress encountered by plants. Plant Molecular Biology Reporter 33(3):347-357. https://doi.org/10.1007/s11105-014-0799-9

Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, … Pachter L (2012). Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols 7(3):562-578. https://doi.org/10.1038/nprot.2012.016

Velez-Ramirez AI, van Ieperen W, Vreugdenhil D, van Poppel P, Heuvelink E, Millenaar FF (2014). A single locus confers tolerance to continuous light and allows substantial yield increase in tomato. Nature Communications 5:4549. https://doi.org/10.1038/ncomms5549

Wang Y, Cai SY, Yin LL, Shi K, Xia XJ, Zhou YH, … Zhou J (2015). Tomato HsfA1a plays a critical role in plant drought tolerance by activating ATG genes and inducing autophagy. Autophagy 11(11):2033-2047. https://doi.org/10.1080/15548627.2015.1098798

Wang L, Feng Z, Wang X, Wang X, Zhang X (2010). DEGseq: an R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 26(1):136-138. https://doi.org/10.1093/bioinformatics/btp612

Wani SH, Tripathi P, Zaid A, Challa GS, Kumar A, Kumar V, … Bhatt M (2018). Transcriptional regulation of osmotic stress tolerance in wheat (Triticum aestivum L.). Plant Molecular Biology 97(6):469-487. https://doi.org/10.1007/s11103-018-0761-6

Wei Y, Wang Y, Wu XY, Shu S, Sun J, Guo SR (2019). Redox and thylakoid membrane proteomic analysis reveals the Momordica (Momordica charantia L.) rootstock-induced photoprotection of cucumber leaves under short-term heat stress. Plant Physiology and Biochemistry 136:98-108. https://doi.org/10.1016/j.plaphy.2019.01.010

Yao Y, He RJ, Xie QL, Zhao XH, Deng XM, He JB, … Wu AM (2017). Ethylene response factor 74 (ERF74) plays an essential role in controlling a respiratory burst oxidase homolog D (RbohD)-dependent mechanism in response to different stresses in Arabidopsis. New Phytologist 213(4):1667-1681. https://doi.org/10.1111/nph.14278

Zhong M, Wang Y, Hou K, Shu S, Sun J, Guo SR (2019a). TGase positively regulates photosynthesis via activation of Calvin cycle enzymes in tomato. Horticulture Research 6:62. https://doi.org/10.1038/s41438-019-0173-z

Zhong M, Wang Y, Zhang Y, Shu S, Sun J, Guo SR (2019b). Overexpression of transglutaminase from cucumber in tobacco increases salt tolerance through regulation of photosynthesis. International Journal of Molecular Sciences 20:894. https://doi.org/10.3390/ijms20040894

Downloads

Additional Files

Published

2021-03-09

How to Cite

JAHAN, M. S., SHI, Z. ., ZHONG, M., ZHANG, Y. ., ZHOU, R. ., EL-MOGY, M. M. ., SUN, J., SHU, S. ., GUO, S., & WANG, Y. . (2021). Comparative transcriptome analysis reveals gene network regulation of TGase-induced thermotolerance in tomato. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 49(1), 12208. https://doi.org/10.15835/nbha49112208

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha49112208