|
Special Issue:
园艺-分子生物合辑Horticulture — Genetics · Breeding
|
|
|
|
| Genome-wide identification and expression analysis of GDSL esterase/lipase genes in tomato |
| SUN Yao-guang, HE Yu-qing, WANG He-xuan, JIANG Jing-bin, YANG Huan-huan, XU Xiang-yang |
School of Horticulture and Landscape Architecture, Northeast Agricultural University, Harbin 150030, P.R.China
|
|
|
|
|
摘要
GDSL酯酶/脂肪酶家族包含许多功能基因，它们在植物的生长发育、形态建成、种子油脂合成和防御反应中发挥重要的生物学功能。GDSL酯酶/脂肪酶基因可响应生物和非生物胁迫。虽然GDSL酯酶/脂肪酶家族基因在其他植物中已被鉴定和研究，但它们在番茄中的分类和功能尚不清楚。本研究首次在番茄中鉴定了80个GDSL酯酶/脂肪酶家族基因成员，命名为SlGELP1-80。我们对这些基因在染色体上的位置进行了定位，并对它们的理化性质、基因结构、系统发育关系、共线关系和顺式作用元件进行了分析。SlGELP基因在番茄中的时空表达特征具有多样性。此外，结合RNA-seq分析表明，番茄接种Stemphylium lycopersici前后SlGELP基因的表达模式不同。用qRT-PCR方法验证了番茄接种S. lycopersici病原菌以及分别喷施SA和JA处理后5个显著差异SlGELP基因的表达。本研究首次利用生物信息学方法鉴定和分析了番茄GDSL酯酶/脂肪酶家族基因，为提高植物抗病性研究提供了新的思路。
Abstract The GDSL esterase/lipase family contains many functional genes that perform important biological functions in growth and development, morphogenesis, seed oil synthesis, and defense responses in plants. The expression of GDSL esterase/lipase genes can respond to biotic and abiotic stresses. Although GDSL esterase/lipase family genes have been identified and studied in other plants, they have not been identified and their functions remain unclear in tomato. This study is the first to identify 80 GDSL esterase/lipase family genes in tomato, which were named SlGELP1–80. These genes were mapped to their positions on the chromosomes and their physical and chemical properties, gene structure, phylogenetic relationships, collinear relationships, and cis-acting elements were analyzed. The spatiotemporal expression characteristics of the SlGELP genes in tomato were diverse. In addition, RNA-seq analysis indicated that the expression patterns of the SlGELP genes in tomato differed before and after inoculation with Stemphylium lycopersici. qRT-PCR was used to analyze the expression of five SlGELP genes after treatments with S. lycopersici, salicylic acid and jasmonic acid. Finally, this study was the first to identify and analyze GDSL esterase/lipase family genes in tomato via bioinformatics approaches, and these findings provide new insights for improving the study of plant disease resistance.
|
|
Received: 02 July 2020
Accepted: 16 October 2020
|
| Fund: This work was supported by the “BaiQianWan” Project of Heilongjiang Province, China (2019ZX16B02), the National Natural Science Foundation of China (32002059), the Heilongjiang Natural Science Foundation of China (LH2020C10), and the Fellowship of China Postdoctoral Science Foundation (2020M681068). |
| About author: SUN Yao-guang, E-mail: 1135312006@qq.com; Correspondence YANG Huan-huan, E-mail: huanyaya0126@sina.com; XU Xiang-yang, Tel/Fax: +86-451-55190748, E-mail: xxy709@126.com |
Cite this article:
SUN Yao-guang, HE Yu-qing, WANG He-xuan, JIANG Jing-bin, YANG Huan-huan, XU Xiang-yang.
2022.
Genome-wide identification and expression analysis of GDSL esterase/lipase genes in tomato. Journal of Integrative Agriculture, 21(2): 389-406.
|
Allah A E F, Hashem A, Ezzat S M. 2006. Lipid metabolism in tomato and bean as a sensitive monitor for biocontrol of wilt diseases. Phytoparasitica, 34, 516–522.
Akoh C C, Lee G C, Liaw Y C, Huang T H, Shaw J F. 2004. GDSL family of serine esterases/lipases. Progress in Lipid Research, 43, 534–552.
An X L, Dong Z Y, Tian Y H, Xie K, Wu S W, Zhu T T, Zhang D F, Zhou Y, Niu C F, Ma B, Hou Q C, Bao J X, Zhang S M, Li Z W, Wang Y B, Yan T W, Sun X J, Zhang Y W, Li J P, Wan X Y. 2019. ZmMs30 encoding a novel GDSL lipase is essential for male fertility and valuable for hybrid breeding in maize. Molecular Plant, 12, 343–359.
Bostock R M, Karban R, Thaler J S, Weyman P D, Gilchrist D. 2001. Signal interactions in induced resistance to pathogens and insect herbivores. European Journal of Plant Pathology, 107, 103–111.
Bu Q, Jiang H, Li C B, Zhai Q, Zhang J, Wu X, Sun J, Xie Q, Li C. 2008. Role of the Arabidopsis thaliana NAC transcription factors ANAC019 and ANAC055 in regulating jasmonic acid-signaled defense responses. Cell Research, 18, 756–767.
Burow M, Zhang Z Y, Ober J A, Lambrix V M, Wittstock U, Gershenzon J, Kliebenstein D J. 2008. ESP and Esm1 mediate indol-3-acetonitrile production from indol-3-ylmethyl glucosinolate in Arabidopsis. Phytochemistry, 69, 663–671.
Cannon S B, Mitra A, Baumgarten A, Young N D, May G. 2004. The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biology, 4, 10.
Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: An integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13, 1194–1202.
Chepyshko H, Lai C P, Huang L M, Liu J H, Shaw J F. 2012. Multifunctionality and diversity of GDSL esterase/lipase gene family in rice (Oryza sativa L. japonica) genome: New insights from bioinformatics analysis. BMC Genomics, 13, 309.
Cui Y, Jing J, Yang H, Zhao T, Xu X, Li J. 2018. Virus-induced gene silencing (VIGS) of the NBS-LRR gene SLNLC1 compromises Sm-mediated disease resistance to Stemphylium lycopersici in tomato. Biochemical and Biophysical Research Communications, 503, 1524–1529.
Dangl J L, Jones J D G. 2001. Plant pathogens and integrated defence responses to infection. Nature, 411, 826–833.
Deyoung B J, Innes R W. 2006. Plant NBS-LRR proteins in pathogen sensing and host defense. Nature Immunology, 7, 1243–1249.
Eulgem T, Rushton P J, Schmelzer E, Hahlbrock K, Somssich I E. 1999. Early nuclear events in plant defence signalling: rapid gene activation by WRKY transcription factors. EMBO Journal, 18, 4689–4699.
Feng C Y, Han J X, Han X X, Jiang J. 2015. Genome-wide identification, phylogeny, and expression analysis of the sweet gene family in tomato. Gene, 573, 261–272.
Finn R D, Clements J, Eddy S R. 2011. HMMER web server: interactive sequence similarity searching. Nucleic Acids Research, 39, 29–37.
Flagel L E, Wendel J F. 2009. Gene duplication and evolutionary novelty in plants. New Phytologist, 183, 557–564.
Franco M E E, Troncozo M I, López S M Y, Lucentini G, Medina R, Saparrat M C N, Ronco L B, Balatti P A. 2017. A survey on tomato leaf grey spot in the two main production areas of Argentina led to the isolation of Stemphylium lycopersici representatives which were genetically diverse and differed in their virulence. European Journal of Plant Pathology Volume, 149, 983–1000.
Gao M, Yin X, Yang W, Lam S M, Tong X, Liu J, Wang X, Li Q, Shui G, He Z. 2017. GDSL lipases modulate immunity through lipid homeostasis in rice. PLoS Pathogens, 13, e1006724.
Godiard L, Grant M R, Dietrich R A, Kiedrowski S, Dangl J L. 1994. Perception and response in plant disease resistance. Current Opinion in Genetics & Development, 4, 662–671.
Gu Z L, Cavalcanti A, Chen F C, Bouman P, Li W H. 2002. Extent of gene duplication in the genomes of drosophila, nematode, and yeast. Molecular Biology and Evolution, 19, 256–262.
Hamamouch N, Li C, Seo P J, Park C M, Davis E L. 2011. Expression of Arabidopsis pathogenesis-related genes during nematode infection. Molecular Plant Pathology, 12, 355–364.
Hong J K, Choi H W, Hwang I S, Kim D S, Kim N H, Choi D S, Kim Y J, Hwang B K. 2008. Function of a novel GDSL-type pepper lipase gene, CaGLIP1, in disease susceptibility and abiotic stress tolerance. Planta, 227, 539–558.
Kim D, Jeannotte R, Welti R, Bockus W W. 2013. Lipid profiles in wheat cultivars resistant and susceptible to tan spot and the effect of disease on the profiles. Phytopathology, 103, 74–80.
Kim H G, Kwon S J, Jang Y J, Chung J H, Nam M H, Park O K. 2014. GDSL lipase 1 regulates ethylene signaling and ethylene-associated systemic immunity in Arabidopsis. FEBS Letters, 588, 1652–1658.
Kim Y. 2004. Cloning and expression of a lipase gene from rice (Oryza sativa cv. Dongjin). Molecules and Cells, 18, 40–45.
Kondou Y, Nakazawa M, Kawashima M, Ichikawa T, Yoshizumi T, Suzuki K, Ishikawa A, Koshi T, Matsui R, Muto S, Matsui M. 2008. RETARDED GROWTH OF EMBRYO1, a new basic helix-loop-helix protein, expresses in endosperm to control embryo growth. Plant Physiology, 147, 1924–1935.
Kong H, Landherr L L, Frohlich M W, Leebens-Mack J, Ma H, dePamphilis C W. 2007. Patterns of gene duplication in the plant SKP1 gene family in angiosperms: evidence for multiple mechanisms of rapid gene birth. Plant Journal, 50, 873–885.
Kong Q, Yang H, Wang Y, Huo D, Hu H, Liu Z, Qin L. 2012. Programmed cell death in plant–pathogen interactions. Plant Protection, 48, 525–545.
Kram B W, Bainbridge E A, Perera M A, Carter C. 2008. Identification, cloning and characterization of a GDSL lipase secreted into the nectar of Jacaranda mimosifolia. Plant Molecular Biology, 68, 173–183.
Kwon S J, Jin H C, Lee S, Nam M H, Chung J H, Kwon S I, Ryu C M, Park O K. 2009. GDSL lipase-like 1 regulates systemic resistance associated with ethylene signaling in Arabidopsis. Plant Journal, 58, 235–245.
Lee D S, Kim B K, Kwon S J, Jin H C, Park O K. 2009. Arabidopsis GDSL lipase 2 plays a role in pathogen defense via negative regulation of auxin signaling. Biochemical and Biophysical Research Communications, 379, 1038–1042.
Lee H J, Park O K. 2019. Lipases associated with plant defense against pathogens. Plant Science, 279, 51–58.
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Peer Y V, Rouzé P, Rombauts S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research, 30, 325–327.
Ling H. 2008. Sequence analysis of GDSL lipase gene family in Arabidopsis thaliana. Pakistan Journal of Biological Sciences, 11, 763–767.
Ling H, Zuo K, Zhao J, Qin J, Qiu C, Sun X, Tang K. 2006. Isolation and characterization of a homologous to lipase gene from Brassica napus. Russian Journal of Plant Physiology, 53, 366–372.
Molineris I, Sales G, Bianchi F, Ferdinando D C, Caselle M. 2010. A new approach for the identification of processed pseudogenes. Journal of Computational Biology, 17, 755–765.
Naranjo M A, Forment J, Roldán M, Serrano R, Vicente O. 2006. Overexpression of Arabidopsis thaliana LTL1, a salt-induced gene encoding a GDSL-motif lipase, increases salt tolerance in yeast and transgenic plants. Plant Cell and Environment, 29, 1890–1900.
Narusaka Y, Nakashima K, Shinwari Z K, Sakuma Y, Furihata F, Abe H, Narusaka M, Shinozaki K, Shinozaki K Y. 2003. Interaction between two cis-acting elements, ABRE and DRE, in ABA-dependent expression of Arabidopsis rd29A gene in response to dehydration and high-salinity stresses. Plant Journal, 34, 137–148.
Ni P Y, Ji X R, Guo D L. 2020. Genome-wide identification, characterization, and expression analysis of GDSL-type esterases/lipases gene family in relation to grape berry ripening. Scientia Horticulturae, 264, 109162.
Ortega A G, Rivera I, Franco S C, Mora A G, Solís A, Hernández C S, Horchani H, Sandoval G. 2017. Identification, cloning and expression of a new GDSL lipase from Carica papaya. Process Biochemistry, 55, 70–76.
Riemann M, Gutjahr C, Korte A, Riemann M, Danger B, Muramatsu T, Bayer U, Waller F, Furuya M, Nick P. 2007. GER1, a GDSL motif-encoding gene from rice is a novel early light- and jasmonate-induced gene. Plant Biology, 9, 32–40.
Roy S W, Penny D. 2007. Patterns of intron loss and gain in plants: Intron loss-dominated evolution and genome-wide comparison of O. sativa and A. thaliana. Molecular Biology and Evolution, 24, 171–181.
Sappl P G, Carroll A J, Clifton R, Lister R, Singh K B. 2010. The Arabidopsis glutathione transferase gene family displays complex stress regulation and co-silencing multiple genes results in altered metabolic sensitivity to oxidative stress. Plant Journal, 58, 53–68.
Scarpari M, Punelli M, Scala V, Zaccaria M, Nobili C, Ludovici M, Camera E, Fabbri A A, Reverberi M, Fanelli C. 2014. Lipids in Aspergillus flavus–maize interaction. Frontiers in Microbiology, 5, 74.
Schmid K M, Ohlrogge J B. 1996. Lipid metabolism in plants. New Comprehensive Biochemistry, 31, 363–389.
Schröder F, Lisso J, Müssig C. 2012. Expression pattern and putative function of exl1 and homologous genes in Arabidopsis. Plant Signaling & Behavior, 7, 22–27.
Serrano M, Coluccia F, Torres M, Haridon L F, Métraux J P. 2014. The cuticle and plant defense to pathogens. Frontiers in Plant Science, 5, 274.
Shah J. 2005. Lipids, lipases, and lipid-modifying enzymes in plant disease resistance. Annual Review of Phytopathology, 43, 229–260.
Su X, Zhu G, Huang Z, Wang X, Guo Y, Du Y, Yang W, Gao J. 2019. Fine mapping and molecular marker development of the Sm gene conferring resistance to gray leaf spot (Stemphylium spp.) in tomato. Theoretical and Applied Genetics, 132, 871–882.
Sun X L, Li Y, Cai H, Bai X, Ji W, Ji Z J, Zhu Y M. 2011. Arabidopsis bZIP1 transcription factor binding to abre cis-element regulates abscisic acid signal transduction. Acta Agronomica Sinica, 37, 612–619. (in Chinese)
Tabata T, Takase H, Takayama S, Mikami K, Nakatsuka A, Kawata T, Nakayama T, Iwabuchi M. 1989. A protein that binds to a cis-acting element of wheat histone genes has a leucine zipper motif. Science, 245, 965–967.
Tanksley S D, Ganal M W, Prince J P, Vicente M C, Bonierbale M W, Broun P, Fulton T M, Giovannoni J J, Grandillo S, Martin G B, Messeguer R, Miller J C, Miller L, Paterson A H, Pineda O, Roder M S, Wing R A, Wu W, Young N D. 1992. High density molecular linkage maps of the tomato and potato genomes. Genetics, 132, 1141–1160.
Updegraff E P, Zhao F, Preuss D. 2009. The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sexual Plant Reproduction, 22, 197–204.
Volokita M, Rosilio-Brami T, Rivkin N, Zik M. 2010. Combining comparative sequence and genomic data to ascertain phylogenetic relationships and explore the evolution of the large GDSL-lipase family in land plants. Molecular Biology and Evolution, 28, 551–565.
Wang Y, Tang H, Debarry J D, Tan X, Li J, Wang X, Lee T, Jin H, Marler B, Guo H, Kissinger J C, Paterson A H. 2012. Mcscanx: A toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Research, 40, e49.
Wang Z Y, Soanes D M, Kershaw M J, Talbot N J. 2007. Functional analysis of lipid metabolism in Magnaporthe grisea reveals a requirement for peroxisomal fatty acid β-oxidation during appressorium-mediated plant infection. Molecular Plant-Microbe Interactions, 20, 475–491.
Wu T, Qin Z W, Zhou X Y, Feng Z, Du Y L. 2010. Transcriptome profile analysis of floral sex determination in cucumber. Journal of Plant Physiology, 169, 905–913.
Yang H, Shen F, Wang H, Zhao T, Zhang H, Xu X, Li J. 2020. Functional analysis of the SlERF01 gene in disease resistance to S. lycopersici. BMC Plant Biology, 20, 376.
Yang H, Zhao T, Jiang J, Chen X, Zhang H, Liu G, Zhang D, Du C, Wang S, Xu X, Li J. 2017. Transcriptome analysis of the sm-mediated hypersensitive response to Stemphylium lycopersici in tomato. Frontiers in Plant Science, 8, 1257.
Yu X, Li L, Zola J, Aluru M, Ye H, Foudree A, Guo H, Anderson S, Aluru S, Liu P, Rodermel S, Yin Y. 2011. A brassinosteroid transcriptional network revealed by genome-wide identification of BESI target genes in Arabidopsis thaliana. Plant Journal, 65, 634–646.
Zhang Y, Wang X, Li Y, Wu L, Zhou H, Zhang G, Ma Z. 2013. Ectopic expression of a novel ser/thr protein kinase from cotton (Gossypium barbadense), enhances resistance to Verticillium dahliae infection and oxidative stress in Arabidopsis. Plant Cell Reports, 32, 1703–1713.
Zhou Y, Hu L F, Jiang L W, Liu S Q. 2018. Genome-wide identification and expression analysis of YTH domain-containing RNA-binding protein family in cucumber (Cucumis sativus). Genes Genomics, 40, 579–589.
|
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
