Gene cloning and expression analyses of WBC genes in the developing grapevine seeds

doi:10.1016/S2095-3119(17)61827-6

摘要/Abstract

摘要： :

Abstract:

White-brown complex (WBC) transporters, also called half-size ATP binding cassette G (ABCG) transporters, are involved in many biological processes, including seed development; however, the WBC transporters in grapevines received less attention to date. To reveal the molecular characteristics of WBCs and the connection between WBCs and agronomic traits of stenospermocarpic (seedless) grapevine, we carried out a genomic census and analysis of ovule-associated expression for VvWBC genes in grapevine. We identified 30 VvWBC genes and cloned full-length complementary DNAs (cDNAs) for 20 of these. The tissue or organ-specific expression analysis showed that several VvWBCs exhibited distinct expression patterns with some showing tissue specificity. Twelve VvWBC genes were found to be expressed in the developing ovules. Moreover, the results of quantitative real-time PCR (qRT-PCR) suggested that four of twelve ovule-expressed VvWBCs have distinct expression profiles during the development of ovules between seeded and stenospermocarpic grapevines. These four genes might be involved in ovule abortion. Meanwhile, chromosome mapping, multiple sequence alignments, exon/intron structure analyses and synteny analyses were preformed on VvWBC genes. Our experiments provide a new perspective on the mechanism of stenospermocarpic seedlessness and put forward a framework for further study of WBC transporters.

Key words:

Vitis vinifera , stenospermocarpy , VvWBCs , half-size VvABCGs , gene cloning , expression analysis

. [J]. Journal of Integrative Agriculture, 2018, 17(06): 1348-1359.

TANG Yu-jin, WANG Qian, XUE Jing-yi, LI Yan, LI Rui-min, Steve Van Nocker, WANG Yue-jin, ZHANG Chao-hong. Gene cloning and expression analyses of WBC genes in the developing grapevine seeds[J]. Journal of Integrative Agriculture, 2018, 17(06): 1348-1359.

参考文献

Adam-Blondon A F, Lahogue-Esnault F, Bouquet A, Boursiquot J M, This P. 2001. Usefulness of two SCAR markers for marker-assisted selection of seedless grapevine cultivars. Vitis, 40, 147–155.
Andolfo G, Ruocco M, Di Donato A, Frusciante L, Lorito M, Scala F, Ercolano M R. 2015. Genetic variability and evolutionary diversification of membrane ABC transporters in plants. BMC Plant Biology, 15, 51.
Banasiak J, Biala W, Staszków A, Swarcewicz B, Kepczynska E, Figlerowicz M, Jasinski M. 2013. A Medicago truncatula ABC transporter belonging to subfamily G modulates the level of isoflavonoids. Journal of Experimental Botany, 64, 1005–1015.
Baud S, Guyon V, Kronenberger J, Wuilleme S, Miquel M, Caboche M, Lepiniec L, Rochat C. 2003. Multifunctional acetyl-CoA carboxylase 1 is essential for very long chain fatty acid elongation and embryo development in Arabidopsis. The Plant Journal, 33, 75–86.
Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu X, Yephremov A, Samuels L. 2007. Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. The Plant Journal, 52, 485–498.
Bonaventure G, Salas J J, Pollard M R, Ohlrogge J B. 2003. Disruption of the FATB gene in Arabidopsis demonstrates an essential role of saturated fatty acids in plant growth. The Plant Cell, 15, 1020–1033.
Buda G J, Barnes W J, Fich E A, Park S, Yeats T H, Zhao L, Domozych D S, Rose J K. 2013. An ATP binding cassette transporter is required for cuticular wax deposition and desiccation tolerance in the moss Physcomitrella patens. The Plant Cell, 25, 4000–4013.
Cakir B, Kilickaya O. 2013. Whole-genome survey of the putative ATP-binding cassette transporter family genes in Vitis vinifera. PLoS ONE, 8, 11.
Chen G, Komatsuda T, Ma J F, Nawrath C, Pourkheirandish M, Tagiri A, Hu Y G, Sameri M, Li X, Zhao X, Liu Y, Li C, Ma X, Wang A, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng X, Nevo E. 2011. An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proceedings of the National Academy of Sciences of the United States of America, 108, 12354–12359.
Chen X, Goodwin S M, Liu X, Bressan R A, Jenks M A. 2005. Mutation of the RESURRECTION1 locus of Arabidopsis reveals an association of cuticular wax with embryo development. Plant Physiology, 139, 909–919.
Chen Z J, Ni Z F. 2006. Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. BioEssays, 28, 240–252.
Choi H, Jin J Y, Choi S, Hwang J U, Kim Y Y, Suh M C, Lee Y. 2011. An ABCG/WBC-type ABC transporter is essential for transportof sporopollenin precursors for exine formation in developing pollen. The Plant Journal, 65, 181–193.
Crouzet J, Roland J, Peeters E, Trombik T, Ducos E, Nader J, Boutry M. 2013. NtPDR1, a plasma membrane ABC transporter from Nicotiana tabacum, is involved in diterpene transport. Plant Molecular Biology, 82,181–192.
Crouzet J, Trombik T, Fraysse A S, Boutry M. 2006. Organization and function of the plant pleiotropic drug resistance ABC transporter family. FEBS Letters, 580, 1123–1130.
Dou X Y, Yang K Z, Zhang Y, Wang W, Liu X L, Chen L Q, Zhang X Q, Ye D. 2011. WBC27, an adenosine tri-phosphate-binding cassette protein, controls pollen wall formation and patterning in Arabidopsis. Journal of Intergrative Plant Biology, 53, 74–88.
Ezaki B, Takahashi K, Utsumi K, Higashi A. 2015. A half-type AvABCG1 transporter derived from Andropogon virginicus L. confers aluminum tolerance. Environmental and Experimental Botany, 118, 21–31.
Fabre G, Garroum I, Mazurek S, Daraspe J, Mucciolo A, Sankar M, Humbel B M, Nawrath C. 2016. The ABCG transporter PEC1/ABCG32 is required for the formation of the developing leaf cuticle in Arabidopsis. New Phytologist, 209, 192–201.
Fang L, Cheng F, Wu J, Wang X W. 2012. Gene retention following whole genome duplication and tandem duplication in Brassica rapa. Biothchnology Bulletin, 11, 9–14. (in Chinese)
Halbrooks M C, Mortensen J A. 1988. Effects of gibberellic acid on berry and seed development in ‘Orlando Seedless’ grape. HortScience, 23, 409.
Higgins C F, Linton K J. 2004. The ATP switch model for ABC transporters. Nature Structural & Molecular Biology, 11, 918–926.
Hwang J U, Song W Y, Hong D, Ko D, Yamaoka Y, Jang S, Yim S, Lee E, Khare D, Kim K, Palmgren M, Yoon H S, Martinoia E, Lee Y. 2016. Plant ABC transporters enable many unique aspects of a terrestrial plant’s lifestyle. Molecular Plant, 9, 338–355.
Jaillon O, Aury J M, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyère C, Billault A, et al. 2007. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature, 449, 463–465.
Kim Y, Park S Y, Kim D, Choi J, Lee Y H, Lee J H, Choi W. 2013. Genome-scale analysis of ABC transporter genes and characterization of the ABCC type transporter genes in Magnaporthe oryzae. Genomics, 101, 354–361.
Kretzschmar T, Kohlen W, Sasse J, Borghi L, Schlegel M, Bachelier J B, Reinhardt D, Bours R, Bouwmeester H J, Martinoia E. 2012. A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching. Nature, 483, 341–344.
Krzywinski M, Schein J, Birol ?, Connors J, Gascoyne R, Horsman D, Jones S J, Marra M A. 2009. Circos: An information aesthetic for comparative genomics. Genome Research, 19, 1639–1645.
Kuromori T, Ito T, Sugimoto E, Shinozaki K. 2011a. Arabidopsis mutant of AtABCG26, an ABC transporter gene, is defective in pollen maturation. Journal of Plant Physiology, 168, 2001–2005.
Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K. 2010. ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proceedings of the National Academy of Sciences of the United States of America, 107, 2361–2366.
Kuromori T, Sugimoto E, Shinozaki K. 2011b. Arabidopsis mutants of AtABCG22, an ABC transporter gene, increase water transpiration and drought susceptibility. The Plant Journal, 67, 885–894.
Le Hir R, Sorin C, Chakraborti D, Moritz T, Schaller H, Tellier F, Robert S, Morin H, Bako L, Bellini C. 2013. ABCG9, ABCG11 and ABCG14 ABC transporters are required for vascular development in Arabidopsis. The Plant Journal, 76, 811–824.
Li L, Li D, Liu S, Ma X, Dietrich C R, Hu H C, Zhang G, Liu Z, Zheng J, Wang G, Schnable P S. 2013. The maize glossy13 gene, cloned via BSR-Seq and Seq-walking encodes a putative ABC transporter required for the normal accumulation of epicuticular waxes. PLoS ONE, 8, e82333.
Li X Q, Yin X G, Wang H, Li J, Guo C L, Gao H, Zheng Y, Fan C H, Wang X P. 2015. Genome-wide identification and analysis of the apple (Malus×domestica Borkh.) TIFY gene family. Tree Genetics & Genomes, 11, 808.
Luo B, Xue X Y, Hu W L, Wang L J, Chen X Y. 2007. An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant and Cell Physiology, 48, 1790–1802.
McFarlane H E, Shin J J, Bird D A, Samuels A L. 2010. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. The Plant Cell, 22, 3066–3075.
Muhovski Y, Jacquemin J M, Batoko H. 2014. Identification and differential induction of ABCG transporter genes in wheat cultivars challenged by a deoxynivalenol producing Fusarium graminearum strain. Molecular Biology Reports, 41, 6181–6194.
Nuruzzaman M, Zhang R, Cao H Z, Luo Z Y. 2014. Plant pleiotropic drug resistance transporters: Transport mechanism, gene expression, and function. Journal of Integrative Plant Biology, 56, 729–740.
Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke R B, Höfer R, Schreiber L, Chory J, Aharoni A. 2007. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiology, 145, 1345–1360.
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.
Panikashvili D, Shi J X, Schreiber L, Aharoni A. 2011. The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytologist, 190, 113–124.
Pighin J A, Zheng H, Balakshin L J, Goodman I P, Western T L, Jetter R, Kunst L, Samuels A L. 2004. Plant cuticular lipid export requires an ABC transporter. Science, 22, 702–704.
Quilichini T D, Friedmann M C, Samuels A L, Douglas C J. 2010. ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiology, 154, 678–690.
Ramnning D W, Emershad R L, Tarllo R. 2000. A Stenospermocarpic, seedless Vitis vinifera×Vitis rotundiyolia hybrid developed by embryo rescue. HortScience, 35, 732–734.
Rapp R A, Wendel J F. 2005. Epigenetics and plant evolution. New Phytologist, 168, 81–91.
Rea P A. 2007. Plant ATP-binding cassette transporters. Annual Review of Plant Biology, 58, 347–375.
Ruocco M, Ambrosino P, Lanzuise S, Woo S L, Lorito M, Scala F. 2011. Four potato (Solanum tuberosum) ABCG transporters and their expression in response to abiotic factors and Phytophthora infestans infection. Journal of Plant Physiology, 168, 2225–2233.
Samuels L, Kunst L, Jetter R. 2008. Sealing plant surfaces: Cuticular wax formation by epidermal cells. Annual Review of Plant Biology, 59, 683–707.
Shibata Y, Ojika M, Sugiyama A, Yazaki K, Jones D A, Kawakita K, Takemoto D. 2016. The full-size ABCG transporters Nb-ABCG1 and Nb-ABCG2 function in pre- and post-invasion defense against Phytophthora infestans in Nicotiana benthamiana. The Plant Cell, 28, 1163–1181.
Smart C C, Fleming A J. 1996. Hormonal and environmental regulation of a plant PDR5-like ABC transporter. The Journal of Biological Chemistry, 271, 19351–19357.
Smith A D, Sumazin P, Xuan Z Y, Zhang M Q. 2006. DNA motifs in human and mouse proximal promoters predict tissue-specific expression. Proceedings of the National Academy of Sciences of the United States of America, 103, 6275–6280.
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725-2729.
Tarr P T, Tarling E J, Bojanic D D, Edwards P A, Baldán A. 2009. Emerging new paradigms for ABCG transporters. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, 1791, 584–593.
Ukitsu H. 2007. Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant and Cell Physiology, 48, 1524–1533.
Van D D C, Tampe R. 2004. How do ABC transporters drive transport. Biological Chemistry, 385, 927–933.
Verrier P J, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea P A, Samuels L, Schulz B, Spalding E J, Yazaki K, Theodoulou F L. 2008. Plant ABC proteins: A unified nomenclature and updated inventory. Trends in Plant Science, 13, 151–159.
Wang D Y, Sung H M, Wang T Y, Huang C J, Yang P, Chang T, Wang Y C, Tseng D L, Wu J P, Lee T C, Shih M C, Li W H. 2007. Expression evolution in yeast genes of single-input modules is mainly due to changes in transacting factors. Genome Research, 17, 1161–1169.
Wang J W, Horiuchi S. 1990. A histological study on the seedlessness in ‘Himrod seedless’ grape. Journal of the Japanese Society for Horticultural Science, 59, 455–462.
Wapinski I, Pfeffer A, Friedman N, Regev A. 2007. Natural history and evolutionary principles of gene duplication in fungi. Nature, 449, 54–61.
Xie X, Wang G, Yang L, Cheng T, Gao J, Wu Y, Xia Q. 2015. Cloning and characterization of a novel Nicotiana tabacum ABC transporter involved in shoot branching. Physiologia Plantarum, 153, 299–306.
Xing Y, Ouyang Z Q, Kapur K, Scott M P, Wong W H. 2007. Assessing the conservation of mammalian gene expression using high-density exon arrays. Molecular Biology and Evolution, 24, 1283–1285.
Xu G X, Guo C C, Shan H Y, Kong H Z. 2012. Divergence of duplicate genes in exon-intron structure. Proceedings of the National Academy of Sciences of the United States of America, 109, 1187–1192.
Xu J, Yang C S, Yuan Z, Zhang D S, Gondwe M Y, Ding Z W, Liang W Q, Zhang D B, Wilson Z A. 2010. The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. The Plant Cell, 22, 91–107.
Yadav V, Molina I, Ranathunge K, Castillo I Q, Rothstein S J, Reed J W. 2014. ABCG transporters are required for suberin and pollen wall extracellular barriers in Arabidopsis. The Plant Cell, 26, 3569–3588.
Yim S, Khare D, Kang J, Hwang J U, Liang W Q, Martinoia E, Zhang D B, Kang B H, Lee Y. 2016. Postmeiotic development of pollen surface layers requires two Arabidopsis ABCG-typetransporters. Plant Cell Reports, 35, 1863–1873.
Zha W J, Li S H, Zhou L, Chen Z J, Liu K, Yang G C, Hu G, He G C, You A Q. 2015. Molecular cloning and expression profile of an ATP-binding cassette (ABC) transporter gene from the hemipteran insect Nilaparvata lugens. Genetics and Molecular Research, 14, 2654–2664.
Zhao G C, Shi J X, Liang W Q, Zhang D B. 2016. ATP binding cassette G transporters and plant male reproduction. Plant Signaling and Behavior, 11, e1136764.
Zhang C H, Gong P J, Wei R, Li S X, Zhang X T, Yu Y H, Wang Y J. 2013. The metacaspase gene family of Vitis vinifera L.: Characterization and differential expression during ovule abortion in stenospermocarpic seedless grapes. Gene, 528, 267–276.
Zhang J J, Wang Y J, Wang X P, Yang K Q, Yang J X. 2003. An improved method for rapidly extracting total RNA from Vitis. Journal of Fruit Science, 20, 178–181. (in Chinese)
Zhang K, Novak O, Wei Z, Gou M, Zhang X, Yu Y, Yang H, Cai Y, Strnad M, Liu C J. 2014. Arabidopsis ABCG14 protein controls the acropetal translocation of root-synthesized cytokinins. Nature Communication, 5, 3274.
Zhang Y C, Gao M, Stacy D S, Zhang J F, Wang H, Wang X P. 2012. Genome-wide identification and analysis of the TIFY gene family in grape. PLoS ONE, 7, e44.
Zhu L, Shi J X, Zhao G C, Zhang D B, Liang W Q. 2013. Post-meiotic deficient anther1 (PDA1) encodes an ABC transporter required for the development of anther cuticle and pollen exine in rice. Journal of Plant Biology, 56, 59–68.