Abstract
The major latex protein/ripening-related protein (MLP/RRP) subfamily is known to be involved in a wide range of biological processes of plant development and various stress responses. However, the biological function of MLP/RRP proteins is still far from being clear and identification of them may provide important clues for understanding their roles. Here, we report a genome-wide evolutionary characterization and gene expression analysis of the MLP family in European Vitis species. A total of 14 members, was found in the grape genome, all of which are located on chromosome 1, where are predominantly arranged in tandem clusters. We have noticed, most surprisingly, promoter-sharing by several non-identical but highly similar gene members to a greater extent than expected by chance. Synteny analysis between the grape and Arabidopsis thaliana genomes suggested that 3 grape MLP genes arose before the divergence of the two species. Phylogenetic analysis provided further insights into the evolutionary relationship between the genes, as well as their putative functions, and tissue-specific expression analysis suggested distinct biological roles for different members. Our expression data suggested a couple of candidate genes involved in abiotic stresses and phytohormone responses. The present work provides new insight into the evolution and regulation of Vitis MLP genes, which represent targets for future studies and inclusion in tolerance-related molecular breeding programs.
Similar content being viewed by others
References
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5′-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24(5):701–713
Biais B, Krisa S, Cluzet S, Da Costa G, Waffo-Teguo P, Mérillon J-M, Richard T (2017) Antioxidant and cytoprotective activities of grapevine stilbenes. J Agric Food Chem 65(24):4952–4960
Cannon SB, Mitra A, Baumgarten A, Young ND, May G (2004) The roles of segmental and tandem gene duplication in the evolution of large gene families in Arabidopsis thaliana. BMC Plant Biol 4(1):10
Cheadle C, Vawter MP, Freed WJ, Becker KG (2003) Analysis of microarray data using Z score transformation. J Mol Diagn 5(2):73–81
Chen J-Y, Dai X-F (2010) Cloning and characterization of the Gossypium hirsutum major latex protein gene and functional analysis in Arabidopsis thaliana. Planta 231(4):861–873
Chin CS, Peluso P, Sedlazeck FJ, Nattestad M, Concepcion GT, Clum A, Dunn C, O’Malley R, Figueroabalderas R, Moralescruz A (2016) Phased diploid genome assembly with single-molecule real-time sequencing. Nat Methods 13(12):1050–1054
Chruszcz M, Ciardiello MA, Osinski T, Majorek KA, Giangrieco I, Font J, Breiteneder H, Thalassinos K, Minor W (2013) Structural and bioinformatic analysis of the kiwifruit allergen Act d 11, a member of the family of ripening-related proteins. Mol Immunol 56(4):794–803
Facchini PJ, Park S-U (2003) Developmental and inducible accumulation of gene transcripts involved in alkaloid biosynthesis in opium poppy. Phytochemistry 64(1):177–186
Fasoli M, Dal Santo S, Zenoni S, Tornielli GB, Farina L, Zamboni A, Porceddu A, Venturini L, Bicego M, Murino V (2012) The grapevine expression atlas reveals a deep transcriptome shift driving the entire plant into a maturation program. Plant Cell 24(9):3489–3505
Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453
Griffing LR, Nessler CL (1989) Immunolocalization of the major latex proteins in developing laticifers of opium poppy (Papaver somniferum). J Plant Physiol 134(3):357–363
Guo D, Wong WS, Xu WZ, Sun FF, Qing DJ, Li N (2011a) Cis-cinnamic acid-enhanced 1 gene plays a role in regulation of Arabidopsis bolting. Plant Mol Biol 75(4–5):481–495
Guo J, Yang X, Weston DJ, Chen JG (2011b) Abscisic acid receptors: past, present and future. J Integr Plant Biol 53(6):469–479
Hammondkosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8(10):1773–1791
He Y, Hao Q, Li W, Yan C, Yan N, Yin P (2014) Identification and characterization of ABA receptors in Oryza sativa. PLoS One 9(4):e95246
Inui H, Sawada M, Goto J, Yamazaki K, Kodama N, Tsuruta H, Eun H (2013) A major latex-like protein is a key factor in crop contamination by persistent organic pollutants. Plant Physiol 161(4):2128–2135
Jaillon O, Aury J-M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–467
Kambiranda D, Katam R, Basha SM, Siebert S (2013) iTRAQ-based quantitative proteomics of developing and ripening muscadine grape berry. J Proteome Res 13(2):555–569
Kimbrough JM, Salinas-Mondragon R, Boss WF, Brown CS, Sederoff HW (2004) The fast and transient transcriptional network of gravity and mechanical stimulation in the Arabidopsis root apex. Plant Physiol 136(1):2790–2805
Konstantinidis KT, Tiedje JM (2004) Trends between gene content and genome size in prokaryotic species with larger genomes. Proc Natl Acad Sci USA 101(9):3160–3165
Kreps J, Wu Y, Chang H, Zhu T, Wang X, Harper JF (2002) Transcriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol 130(4):2129–2141
Kuroi T, Nakamoto K (2003) Two different novel cis-acting elements of erd1, a clpA homologous Arabidopsis gene function in induction by dehydration stress and dark-induced senescence. Plant J 33(2):259–270
Kutchan TM (2005) A role for intra-and intercellular translocation in natural product biosynthesis. Curr Opin Plant Biol 8(3):292–300
Lcvan L, Eavan S (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55(2):85–97
Lebel S, Schellenbaum P, Walter B, Maillot P (2010) Characterisation of the Vitis vinifera PR10 multigene family. BMC Plant Biol 10(1):184–184
Lee EJ, Facchini P (2010) Norcoclaurine synthase is a member of the pathogenesis-related 10/Bet v1 protein family. Plant Cell 22(10):3489
Lee O-R, Sathiyaraj G, Kim Y-J, In J-G, Kwon W-S, Kim J-H, Yang D-C (2011) Defense genes induced by pathogens and abiotic stresses in Panax ginseng CA Meyer. J Ginseng Res 35(1):1–11
Litholdo CG, Parker BL, Eamens AL, Larsen MR, Cordwell SJ, Waterhouse PM (2016) Proteomic identification of putative microRNA394 target genes in Arabidopsis thaliana identifies major latex protein family members critical for normal development. Mol Cell Proteom 15(6):2033–2047
Livak KJ, Schmittgen TD (2012) Analysis of relative gene expression data using real-time quantitative PCR and the 2– ∆∆CT method. Methods 25(4):402–408
Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401–1404
Lytle BL, Song J, de la Cruz NB, Peterson FC, Johnson KA, Bingman CA, Phillips GN, Volkman BF (2009) Structures of two Arabidopsis thaliana major latex proteins represent novel helix-grip folds. Proteins 76(1):237–243
Marković-Housley Z, Degano M, Lamba D, von Roepenack-Lahaye E, Clemens S, Susani M, Ferreira F, Scheiner O, Breiteneder H (2003) Crystal structure of a hypoallergenic isoform of the major birch pollen allergen Bet v 1 and its likely biological function as a plant steroid carrier. J Mol Biol 325(1):123–133
Nam Y-W, Tichit L, Leperlier M, Cuerq B, Marty I, Lelièvre J-M (1999) Isolation and characterization of mRNAs differentially expressed during ripening of wild strawberry (Fragaria vesca L.) fruits. Plant Mol Biol 39(3):629–636
Nawrot R, Lippmann R, Matros A, Musidlak O, Nowicki G, Mock H-P (2017) Proteomic comparison of Chelidonium majus L. latex in different phases of plant development. Plant Physiol Biochem 112:312–325
Nessler CL, Burnett RJ (1992) Organization of the major latex protein gene family in opium poppy. Plant Mol Biol 20(4):749–752
Nessler CL, Allen RD, Galewsky S (1985) Identification and characterization of latex-specific proteins in opium poppy. Plant Physiol 79(2):499–504
Nessler CL, Kurz WG, Pelcher LE (1990) Isolation and analysis of the major latex protein genes of opium poppy. Plant Mol Biol 15(6):951–953
Niu D-K, Jiang L (2013) Can ENCODE tell us how much junk DNA we carry in our genome? Biochem Biophys Res Commun 430(4):1340–1343
Osmark P, Boyle B, Brisson N (1998) Sequential and structural homology between intracellular pathogenesis-related proteins and a group of latex proteins. Plant Mol Biol 38(6):1243–1246
Qu Z-L, Wang H-Y, Xia G-X (2005) GhHb1: a nonsymbiotic hemoglobin gene of cotton responsive to infection by Verticillium dahliae. Biochim Biophys Acta 1730(2):103–113
Radauer C, Lackner P, Breiteneder H (2008) The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evol Biol 8(1):286
Rebeiz M, Posakony JW (2004) GenePalette: a universal software tool for genome sequence visualization and analysis. Dev Biol 271(2):431–438
Ruperti B, Bonghi C, Ziliotto F, Pagni S, Rasori A, Varotto S, Tonutti P, Giovannoni JJ, Ramina A (2002) Characterization of a major latex protein (MLP) gene down-regulated by ethylene during peach fruitlet abscission. Plant Sci 163(2):265–272
Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425
Siu-Ming Y, Wong Thomas KF, Zhao M, Ping N, Yang W, Yu L (2008) Promoter-sharing by different genes in human genome—CPNE1 and RBM12 gene pair as an example. BMC Genom 9(1):456
Stanley Kim H, Yu Y, Snesrud EC, Moy LP, Linford LD, Haas BJ, Nierman WC, Quackenbush J (2005) Transcriptional divergence of the duplicated oxidative stress-responsive genes in the Arabidopsis genome. Plant J 41(2):212–220
Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28(10):2731–2739
Thompson JD, Gibson T, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi0203s00
Van LL, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44(1):135–162
Venturini L, Ferrarini A, Zenoni S, Tornielli GB, Fasoli M, Dal SS, Minio A, Buson G, Tononi P, Zago ED (2013) De novo transcriptome characterization of Vitis vinifera cv. Corvina unveils varietal diversity. BMC Genom 14(1):41
Verma V, Raju SC, Kapley A, Kalia VC, Daginawala HF, Purohit HJ (2010) Evaluation of genetic and functional diversity of Stenotrophomonas isolates from diverse effluent treatment plants. Bioresour Technol 101(20):7744–7753
Wang Y, Yang L, Chen X, Ye T, Zhong B, Liu R, Wu Y, Chan Z (2015) Major latex protein-like protein 43 (MLP43) functions as a positive regulator during abscisic acid responses and confers drought tolerance in Arabidopsis thaliana. J Exp Bot 67(1):421–434
Weid M, Ziegler J, Kutchan TM (2004) The roles of latex and the vascular bundle in morphine biosynthesis in the opium poppy, Papaver somniferum. Proc Natl Acad Sci USA 101(38):13957–13962
Wu JM, Wang Z-R, Hsieh T-C, Bruder JL, Zou J-G, Huang Y-Z (2001) Mechanism of cardioprotection by resveratrol, a phenolic antioxidant present in red wine. Int J Mol Med 8(1):3–17
Xu W, Li R, Zhang N, Ma F, Jiao Y, Wang Z (2014) Transcriptome profiling of Vitis amurensis, an extremely cold-tolerant Chinese wild Vitis species, reveals candidate genes and events that potentially connected to cold stress. Plant Mol Biol 86(4–5):527–541
Yang X, Tuskan GA (2006) Divergence of the Dof gene families in poplar, Arabidopsis, and rice suggests multiple modes of gene evolution after duplication. Plant Physiol 142(3):820–830
Yang X, Kalluri UC, Jawdy S, Gunter LE, Yin T, Tschaplinski TJ, Weston DJ, Ranjan P, Tuskan GA (2008) The F-box gene family is expanded in herbaceous annual plants relative to woody perennial plants. Plant Physiol 148(3):1189–1200
Yang C-L, Liang S, Wang H-Y, Han L-B, Wang F-X, Cheng H-Q, Wu X-M, Qu Z-L, Wu J-H, Xia G-X (2015) Cotton major latex protein 28 functions as a positive regulator of the ethylene responsive factor 6 in defense against Verticillium dahliae. Mol Plant. 8(3): 399–411
Ye N, Jia L, Zhang J (2012) ABA signal in rice under stress conditions. Rice 5(1):1–9
Ye CY, Li T, Yin H, Weston DJ, Tuskan GA, Tschaplinski TJ, Yang X (2013) Evolutionary analyses of non-family genes in plants. Plant J 73(5):788–797
Acknowledgements
This study was funded by the Western First-class Discipline Construction Project of Horticulture (Grant Number NXYLXK2017B03), the Major Science and Technology Program of Ningxia Hui Autonomous Region (Grant Number 2016BZ06) and National Natural Science Foundation of China (Grant Number 31560550).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Ethical standards
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by S. Hohmann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Table S1
List of primer-sets of VvMLP genes for qRT-PCR (XLS 23 KB)
Supplementary Table S2
Amino acid identity of MLP gene family between Arabidopsis and V. vinifera cv. Pinot Noir (XLSX 14 KB)
Supplementary Table S3
Amino acid identity between VvMLP gene family (XLSX 10 KB)
Supplementary Table S4
Nucleotide identity of MLP genes between V. vinifera cv. Cabernet Sauvignon (VvcsMLPs) and cv. Pinort Noir (VvpnMLPs) (XLSX 14 KB)
Supplementary Table S5
Promoter sequence identity of MLP genes between V. vinifera cv. Cabernet Sauvignon (VvcsMLPs) and cv. Pinort Noir (VvpnMLPs) (XLSX 11 KB)
Supplementary Table S6
Microarray data of V. vinifera cv. Corvina was retrieved from Grape eFP Browser microarray database (XLS 30 KB)
Rights and permissions
About this article
Cite this article
Zhang, N., Li, R., Shen, W. et al. Genome-wide evolutionary characterization and expression analyses of major latex protein (MLP) family genes in Vitis vinifera. Mol Genet Genomics 293, 1061–1075 (2018). https://doi.org/10.1007/s00438-018-1440-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-018-1440-7