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Journal of Integrative Agriculture  2020, Vol. 19 Issue (5): 1170-1185    DOI: 10.1016/S2095-3119(19)62776-0
Special Issue: Triticeae Crops Genetics · Breeding · Germplasm Resources
Crop Science Advanced Online Publication | Current Issue | Archive | Adv Search |
Bioinformatic identification and analyses of the non-specific lipid transfer proteins in wheat
FANG Zheng-wu1, HE Yi-qin1, LIU Yi-ke2, JIANG Wen-qiang1, SONG Jing-han1, WANG Shu-ping1, MA Dong-fang1, 3, YIN Jun-liang1  
1 Hubei Collaborative Innovation Center for Grain Industry/Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education/Hubei Engineering Research Center for Pest Forewarning and Management/College of Agriculture, Yangtze University, Jingzhou 434025, P.R.China
2 Institute of Food Crops, Hubei Academy of Agricultural Sciences, Wuhan 430064, P.R.China
3 Institute of Plant Protection, Sichuan Academy of Agricultural Sciences/Key Laboratory of Integrated Pest Management of Crop in Southwest China, Ministry of Agriculture and Rural Affairs, Chengdu 610066, P.R.China
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Abstract  
Non-specific lipid transfer proteins (nsLTPs/LTPs) that can transport various phospholipids across the membrane in vitro are widespread in the plant kingdom, and they play important roles in many biological processes that are closely related to plant growth and development.  Recently, nsLTPs have been shown to respond to different forms of abiotic stresses.  Despite the vital roles of nsLTPs in many plants, little is known about the nsLTPs in wheat.  In this study, 330 nsLTP proteins were identified in wheat and they clustered into five types (1, 2, c, d, and g) by phylogenetic analysis with the nsLTPs from maize, Arabidopsis, and rice.  The wheat nsLTPs of type d included three subtypes (d1, d2, and d3) and type g included seven subtypes (g1–g7).  Genetic structure and motif pattern analyses showed that members of each type had similar structural composition.  Moreover, GPI-anchors were found to exist in non-g type members from wheat for the first time.  Chromosome mapping revealed that all five types were unevenly and unequally distributed on 21 chromosomes.  Furthermore, gene duplication events contributed to the proliferation of the nsLTP genes.  Large-scale data mining of RNA-seq data covering multiple growth stages and numerous stress treatments showed that the transcript levels of some of the nsLTP genes could be strongly induced by abiotic stresses, including drought and salinity, indicating their potential roles in mediating the responses of the wheat plants to these abiotic stress conditions.  These findings provide comprehensive insights into the nsLTP family members in wheat, and offer candidate nsLTP genes for further studies on their roles in stress resistance and potential for improving wheat breeding programs.
 
Keywords:  nsLTP        abiotic stress        wheat genome        bioinformatics        gene family  
Received: 29 January 2019   Accepted: 25 March 2020
Fund: This work was supported by the National Transgenic Key Project of the Ministry of Agriculture of China (2018ZX0800909B), the Major Program of Technological Innovation of Hubei Province, China (2018ABA085), the Open Project Program of Engineering Research Center of Ecology and Agricultural Use of Wetland, Ministry of Education, China (KF201802), and the Southwest Agricultural Crop Pest Management Key Laboratory Open Fund of Ministry of Agriculture, China (2018-XNZD-01).
Corresponding Authors:  Correspondence MA Dong-fang, Tel: +86-716-8066302, E-mail: madf@yangtzeu.edu.cn; YIN Jun-liang, Tel: +86-716-8066302, E-mail: yinjunliang@nwafu.edu.cn    

Cite this article: 

FANG Zheng-wu, HE Yi-qin, LIU Yi-ke, JIANG Wen-qiang, SONG Jing-han, WANG Shu-ping, MA Dong-fang, YIN Jun-liang. 2020. Bioinformatic identification and analyses of the non-specific lipid transfer proteins in wheat. Journal of Integrative Agriculture, 19(5): 1170-1185.

Ahmed S M, Peng L, Qinghe X, Changan J, Tuo Q, Jia G. 2017. Tadir1-2, a wheat ortholog of lipid transfer protein atdir1 contributes to negative regulation of wheat resistance against Puccinia striiformis f. sp. tritici. Frontiers in Plant Science, 8, 1–16.
Alaux M, Rogers J, Letellier T, Flores R, Alfama F, Pommier C, Mohellibi N, Durand S, Kimmel E, Michotey C, Guerche C, Loaec M, Lainé M. 2018. Linking the international wheat genome sequencing consortium bread wheat reference genome sequence to wheat genetic and phenomic data. Genome Biology, 19, 111.
Andorf C M, Cannon E K, Portwood J L, Gardiner J M, Harper L C, Schaeffer M L, Braun B L, Campbell D A, Vinnakota A G, Sribalusu V V. 2015. MaizeGDB update: New tools, data and interface for the maize model organism database. Nucleic Acids Research, 44, 1195–1201.
Aramrak A, Kidwell K K, Steber C M, Burke I C. 2015. Molecular and phylogenetic characterization of the homoeologous epsp synthase genes of allohexaploid wheat, Triticum aestivum (L.). BMC Genomics, 16, 844.
Berardini T Z, Reiser L, Li D, Mezheritsky Y, Muller R, Strait E, Huala E. 2015. The Arabidopsis information resource: making and mining the “gold standard” annotated reference plant genome. Genesis, 53, 474–485.
Berecz B, Mills E N C, Tamas L. 2010. Structural stability and surface activity of sunflower 2s albumins and nonspecific lipid transfer protein. Journal of Agricultural and Food Chemistry, 58, 6490.
Boutrot F, Chantret N, Gautier M F. 2008. Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLTP) gene families and identification of wheat nsLTP genes by EST data mining. BMC Genomics, 9, 1–19.
Chou K C, Shen H B. 2010. Plant-mPLoc: A top-down strategy to augment the power for predicting plant protein subcellular localization. PLoS ONE, 5, e11335.
Debono A, Yeats T H, Rose J K, Bird D, Jetter R, Kunst L, Samuels L. 2009. Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. The Plant Cell, 21, 1230–1238.
Deeken R, Saupe S, Klinkenberg J, Riedel M, Leide J, Hedrich R, Mueller T D. 2016. The nonspecific lipid transfer protein atltpi-4 is involved in suberin formation of Arabidopsis thaliana crown galls. Plant Physiology, 172, 1911.
Douliez J P, Michon T, Elmorjani K, Marion D. 2000. Structure, biological and technological functions of lipid transfer proteins and indolines, the major lipid binding proteins from cereal kernels. Journal of Cereal Science, 32, 1–20.
Edstam M M, Laurila M, Andrey H, Raman A, Käthe M D, Salminen T A, Edqvista J, Blomqvista K. 2014. Characterization of the GPI-anchored lipid transfer proteins in the moss Physcomitrella patens. Plant Physiology and Biochemistry, 75, 55–69.
Edstam M M, Viitanen L, Salminen T A, Edqvist J. 2011. Evolutionary history of the non-specific lipid transfer proteins. Molecular Plant, 4, 947–964.
Fankhauser N, Maser P. 2005. Identification of GPI anchor attachment signals by a Kohonen self-organizing map. Bioinformatics, 21, 1846–1852.
Guo L, Yang H, Zhang X, Yang S. 2013. Lipid transfer protein 3
as a target of MYB96 mediates freezing and drought stress in Arabidopsis. Journal of Experimental Botany, 64, 1755–1767.
Hu L, Liu S. 2011. Genome-wide identification and phylogenetic analysis of the ERF gene family in cucumbers. Genetics and Molecular Biology, 34, 624–633.
Hu L P, Zhang F, Song S H, Tang X W, Xu H, Liu G M, Wang Y Q, He H J. 2017. Genome-wide identification, characterization, and expression analysis of the SWEET gene family in cucumber. Journal of Integrative Agriculture, 16, 1486–1501.
Huang M D, Chen T L L, Huang A H C. 2013. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiology, 163, 1218–1229.
Jang C S, Lee H, Chang S J, Seo Y W. 2004. Expression and promoter analysis of the TaLTP1 gene induced by drought and salt stress in wheat (Triticum aestivum L.). Plant Science, 167, 995–1001.
Kader J C. 1996. Lipid-transfer proteins in plants. Annual Review of Plant Physiology and Plant Molecular Biology, 47, 627–654.
Kelley L A, Mezulis S, Yates C M, Wass M N, Sternberg M J E. 2015. The Phyre2 web portal for protein modeling, prediction and analysis. Nature Protocols, 10, 845–858.
Kumar S, Stecher G, Tamura K. 2016. MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology Evolution, 33, 1870.
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y. 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.
Letunic I, Bork P. 2018. 20 years of the SMART protein domain annotation resource. Nucleic Acids Research, 46, D493–D496.
Li B, Yu D W, Zhao F L, Pang C Y, Song M Z, Wei H L, Fan S L, Yu S X. 2015. Genome-wide analysis of the calcium-dependent protein kinase gene family in Gossypium raimondii. Journal of Integrative Agriculture, 14, 29–41.
Li R, An J P, You C X, Shu J, Wang X F, Hao Y J. 2018. Identification and expression of the CEP gene family in apple (Malus×domestica). Journal of Integrative Agriculture, 17, 348–358.
Lovell S C, Davis I W, Arendall R W, Bakker P I, Word J M, Prisant M G, Richardson J S, Richardson D C. 2003. Structure validation by calpha geometry: Phi, psi and cbeta deviation. Proteins-structure Function and Bioinformatics, 50, 437–450.
Matilde J E, Gomis R F X, Pere P. 2004. The eight-cysteine motif, a versatile structure in plant proteins. Plant Physiology and Biochemistry (Paris), 42, 355–365.
Osakabe Y, Yamaguchi-Shinozaki K, Shinozaki K, Tran L S. 2014. ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytologist, 202, 35–49.
Ouyang S, Zhu W, Hamilton J, Lin H, Campbell M, Childs K, Thibaudnissen F, Malek R L, Lee Y, Zheng L. 2007. The TIGR rice genome annotation resource: Improvements and new features. Nucleic Acids Research, 35, 883–887.
Panchy N, Lehtishiu M, Shiu S H. 2016. Evolution of gene duplication in plants. Plant Physiology, 171, 2294.
Panikashvili D, Shi J X, Bocobza S, Franke R B, Schreiber L, Aharoni A. 2010. The Arabidopsis dso/abcg11 transporter affects cutin metabolism in reproductive organs and suberin in roots. Molecular Plant, 3, 563–575.
Pii Y, Astegno A, Peroni E, Zaccardelli M, Pandolfini T, Crimi M. 2009. The Medicago truncatula N5 gene encoding a root-specific lipid transfer protein is required for the symbiotic interaction with Sinorhizobium meliloti. Molecular Plant-Microbe Interactions, 22, 1577–1587.
Rogers R L, Cridland J M, Shao L, Hu T T, Andolfatto P, Thornton K R. 2014. Landscape of standing variation for tandem duplications in Drosophila yakuba and Drosophila simulans. Molecular Biology and Evolution, 31, 1750–1766.
Rogers R L, Ling S, Thornton K R, Begun D J. 2017. Tandem duplications lead to novel expression patterns through exon shuffling in Drosophila yakuba. PLoS Genetics, 13, e1006795.
Sabine J, Jutta L M. 2016. Response of Arabidopsis thaliana roots with altered lipid transfer protein (LTP) gene expression to the clubroot disease and salt stress. Plants, 5, 2.
Salminen T A, Blomqvist K, Edqvist J. 2016. Lipid transfer proteins: Classification, nomenclature, structure, and function. Planta, 244, 971–997.
Schmitt A J, Sathoff A E, Catherine H, Brittany B, Samac D A, Carter C J. 2018. The major nectar protein of Brassica rapa is a non-specific lipid transfer protein, BrLTP2.1, with strong antifungal activity. Journal of Experimental Botany, 69, 5587–5597.
Seo P J, Lee S B, Suh M C, Park M J, Go Y S, Park C M. 2011. The MYB96 transcription factor regulates cuticular wax biosynthesis under drought conditions in Arabidopsis. The Plant Cell, 23, 1138–1152.
Sun J Y, Gaudet D A, Lu Z X, Frick M, Puchalski B, Laroche A. 2008. Characterization and antifungal properties of wheat nonspecific lipid transfer proteins. Molecular Plant-Microbe Interactions, 21, 346–360.
Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley D R, Pimentel H, Salzberg S L, Rinn J L, Pachter L. 2012. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nature Protocols, 7, 562–578.
Thompson J D, Higgins D G, Gibson T J. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 22, 4673–4680.
Ulmasov T, Hagen G, Guilfoyle T J. 1997. ARF1, a transcription factor that binds to auxin response elements. Science, 276, 1865–1868.
Wei K, Zhong X. 2014. Non-specific lipid transfer proteins in maize. BMC Plant Biology, 14, 281.
Yeats T H, Rose J K C. 2008. The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Science, 17, 191–198.
Yin J, Jia J, Lian Z, Hu Y, Guo J, Huo H, Zhu Y, Gong H.  2019. Silicon enhances the salt tolerance of cucumber through increasing polyamine accumulation and decreasing oxidative damage. Ecotoxicology and Environmental Safety, 169, 8–17.
Yin J, Liu M, Ma D, Wu J, Li S, Zhu Y, Han B. 2018. Identification of circular RNAs and their targets during tomato fruit ripening. Postharvest Biology and Technology, 136, 90–98.
Yin J L, Fang Z W, Sun C, Zhang P, Zhang X, Lu C, Wang S P, Ma D F, Zhu Y X. 2018. Rapid identification of a stripe rust resistant gene in a space-induced wheat mutant using specific locus amplified fragment (SLAF) sequencing. Scientific Reports, 8, 3086.
Zhang X W, Yi D X, Shao L H, Li C. 2017. In silico genome-wide identification, phylogeny and expression analysis of the R2R3-MYB gene family in Medicago truncatula. Journal of Integrative Agriculture, 16, 1576–1591.
Zhang Z Y, Zhao J, Hu Y, Zhang Z T. 2015. Isolation of GhMYB9, gene promoter and characterization of its activity in transgenic cotton. Biologia Plantarum, 59, 629–636.
Zhu Y, Gong H. 2014. Beneficial effects of silicon on salt and drought tolerance in plants. Agronmy for Sustainable Development, 34, 455–472.
Zhu Y X, Xu X B, Hu Y H, Han W H, Yin J L, Li H L, Gong H J. 2015. Silicon improves salt tolerance by increasing root water uptake in Cucumis sativus L. Plant Cell Reports, 34, 1629–1646.
Zhu Y, Gong H, Yin J. 2019a. Role of silicon in mediating salt tolerance in plants: A review. Plant, 8, 147.
Zhu Y, Jia J, Yang L, Xia Y, Zhang H, Jia J, Zhou R, Nie P, Yin J, Ma D. 2019b. Identification of cucumber circular RNAs responsive to salt stress. BMC Plant Biology, 19, 164.
Zhu Y, Yin J, Liang Y, Liu J, Jia J, Huo H, Wu Z, Yang R, Gong H. 2019c. Transcriptomic dynamics provide an insight into the mechanism for silicon-mediated alleviation of salt stress in cucumber plants. Ecotoxicology and Environmental Safety, 174, 245–254.
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