Molecular Genetics and Genomics

, Volume 293, Issue 5, pp 1061–1075 | Cite as

Genome-wide evolutionary characterization and expression analyses of major latex protein (MLP) family genes in Vitis vinifera

  • Ningbo Zhang
  • Ruimin Li
  • Wei Shen
  • Shuzhen Jiao
  • Junxiang ZhangEmail author
  • Weirong XuEmail author
Original Article


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.


Vitis·major latex protein and ripening-related protein (MLP/RRP) Phylogenetic analysis Environmental stress Expression analysis 



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).

Compliance with ethical standards

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.

Supplementary material

438_2018_1440_MOESM1_ESM.xls (23 kb)
Supplementary Table S1 List of primer-sets of VvMLP genes for qRT-PCR (XLS 23 KB)
438_2018_1440_MOESM2_ESM.xlsx (14 kb)
Supplementary Table S2 Amino acid identity of MLP gene family between Arabidopsis and V. vinifera cv. Pinot Noir (XLSX 14 KB)
438_2018_1440_MOESM3_ESM.xlsx (11 kb)
Supplementary Table S3 Amino acid identity between VvMLP gene family (XLSX 10 KB)
438_2018_1440_MOESM4_ESM.xlsx (15 kb)
Supplementary Table S4 Nucleotide identity of MLP genes between V. vinifera cv. Cabernet Sauvignon (VvcsMLPs) and cv. Pinort Noir (VvpnMLPs) (XLSX 14 KB)
438_2018_1440_MOESM5_ESM.xlsx (11 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)
438_2018_1440_MOESM6_ESM.xls (30 kb)
Supplementary Table S6 Microarray data of V. vinifera cv. Corvina was retrieved from Grape eFP Browser microarray database (XLS 30 KB)


  1. 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):701–713CrossRefPubMedGoogle Scholar
  2. 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):4952–4960CrossRefPubMedGoogle Scholar
  3. 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):10CrossRefPubMedPubMedCentralGoogle Scholar
  4. Cheadle C, Vawter MP, Freed WJ, Becker KG (2003) Analysis of microarray data using Z score transformation. J Mol Diagn 5(2):73–81CrossRefPubMedPubMedCentralGoogle Scholar
  5. 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):861–873CrossRefPubMedGoogle Scholar
  6. 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):1050–1054CrossRefPubMedPubMedCentralGoogle Scholar
  7. 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):794–803CrossRefPubMedPubMedCentralGoogle Scholar
  8. Facchini PJ, Park S-U (2003) Developmental and inducible accumulation of gene transcripts involved in alkaloid biosynthesis in opium poppy. Phytochemistry 64(1):177–186CrossRefPubMedGoogle Scholar
  9. 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):3489–3505CrossRefPubMedPubMedCentralGoogle Scholar
  10. Freeling M (2009) Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu Rev Plant Biol 60:433–453CrossRefPubMedGoogle Scholar
  11. Griffing LR, Nessler CL (1989) Immunolocalization of the major latex proteins in developing laticifers of opium poppy (Papaver somniferum). J Plant Physiol 134(3):357–363CrossRefGoogle Scholar
  12. 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):481–495CrossRefPubMedGoogle Scholar
  13. Guo J, Yang X, Weston DJ, Chen JG (2011b) Abscisic acid receptors: past, present and future. J Integr Plant Biol 53(6):469–479CrossRefPubMedGoogle Scholar
  14. Hammondkosack KE, Jones JD (1996) Resistance gene-dependent plant defense responses. Plant Cell 8(10):1773–1791CrossRefGoogle Scholar
  15. 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):e95246CrossRefPubMedPubMedCentralGoogle Scholar
  16. 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):2128–2135CrossRefPubMedPubMedCentralGoogle Scholar
  17. 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):463–467CrossRefPubMedGoogle Scholar
  18. 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):555–569CrossRefPubMedPubMedCentralGoogle Scholar
  19. 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):2790–2805CrossRefPubMedPubMedCentralGoogle Scholar
  20. 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):3160–3165CrossRefPubMedGoogle Scholar
  21. 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):2129–2141CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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):259–270CrossRefGoogle Scholar
  23. Kutchan TM (2005) A role for intra-and intercellular translocation in natural product biosynthesis. Curr Opin Plant Biol 8(3):292–300CrossRefPubMedGoogle Scholar
  24. 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):85–97CrossRefGoogle Scholar
  25. Lebel S, Schellenbaum P, Walter B, Maillot P (2010) Characterisation of the Vitis vinifera PR10 multigene family. BMC Plant Biol 10(1):184–184CrossRefPubMedPubMedCentralGoogle Scholar
  26. Lee EJ, Facchini P (2010) Norcoclaurine synthase is a member of the pathogenesis-related 10/Bet v1 protein family. Plant Cell 22(10):3489CrossRefPubMedPubMedCentralGoogle Scholar
  27. 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):1–11CrossRefGoogle Scholar
  28. 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):2033–2047CrossRefGoogle Scholar
  29. Livak KJ, Schmittgen TD (2012) Analysis of relative gene expression data using real-time quantitative PCR and the 2– ∆∆CT method. Methods 25(4):402–408CrossRefGoogle Scholar
  30. Lynch M, Conery JS (2003) The origins of genome complexity. Science 302(5649):1401–1404CrossRefPubMedGoogle Scholar
  31. 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):237–243CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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):123–133CrossRefPubMedGoogle Scholar
  33. 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):629–636CrossRefPubMedGoogle Scholar
  34. 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 112:312–325CrossRefPubMedGoogle Scholar
  35. Nessler CL, Burnett RJ (1992) Organization of the major latex protein gene family in opium poppy. Plant Mol Biol 20(4):749–752CrossRefPubMedGoogle Scholar
  36. Nessler CL, Allen RD, Galewsky S (1985) Identification and characterization of latex-specific proteins in opium poppy. Plant Physiol 79(2):499–504CrossRefPubMedPubMedCentralGoogle Scholar
  37. Nessler CL, Kurz WG, Pelcher LE (1990) Isolation and analysis of the major latex protein genes of opium poppy. Plant Mol Biol 15(6):951–953CrossRefPubMedGoogle Scholar
  38. 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):1340–1343CrossRefPubMedGoogle Scholar
  39. 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):1243–1246CrossRefPubMedGoogle Scholar
  40. 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):103–113CrossRefPubMedGoogle Scholar
  41. 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):286CrossRefPubMedPubMedCentralGoogle Scholar
  42. Rebeiz M, Posakony JW (2004) GenePalette: a universal software tool for genome sequence visualization and analysis. Dev Biol 271(2):431–438CrossRefPubMedGoogle Scholar
  43. 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):265–272CrossRefGoogle Scholar
  44. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4(4):406–425PubMedGoogle Scholar
  45. 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):456CrossRefGoogle Scholar
  46. 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):212–220CrossRefPubMedGoogle Scholar
  47. 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):2731–2739CrossRefPubMedPubMedCentralGoogle Scholar
  48. Thompson JD, Gibson T, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform. CrossRefGoogle Scholar
  49. Van LL, Rep M, Pieterse CM (2006) Significance of inducible defense-related proteins in infected plants. Annu Rev Phytopathol 44(1):135–162CrossRefGoogle Scholar
  50. 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):41CrossRefGoogle Scholar
  51. 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):7744–7753CrossRefPubMedGoogle Scholar
  52. 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):421–434CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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):13957–13962CrossRefPubMedGoogle Scholar
  54. 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):3–17PubMedGoogle Scholar
  55. 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):527–541CrossRefPubMedGoogle Scholar
  56. 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):820–830CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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):1189–1200CrossRefPubMedPubMedCentralGoogle Scholar
  58. 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): 399–411CrossRefPubMedGoogle Scholar
  59. Ye N, Jia L, Zhang J (2012) ABA signal in rice under stress conditions. Rice 5(1):1–9CrossRefPubMedPubMedCentralGoogle Scholar
  60. 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):788–797CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.School of AgronomyNingxia UniversityYinchuanPeople’s Republic of China
  2. 2.Ningxia Engineering and Technology Research Center of Grape and WineNingxia UniversityYinchuanPeople’s Republic of China
  3. 3.Engineering Research Center of Grape and Wine, Ministry of EducationNingxia UniversityYinchuanPeople’s Republic of China
  4. 4.School of Vine and WineNingxia UniversityYinchuanPeople’s Republic of China

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