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Current Genomics

Editor-in-Chief

ISSN (Print): 1389-2029
ISSN (Online): 1875-5488

Research Article

Transcriptomic Analysis Reveals Key Candidate Genes Related to Seed Abortion in Chinese Jujube (Ziziphus jujuba Mill)

Author(s): Fengxia Shao, Hengfu Yin, Sen Wang*, Saiyang Zhang, Juan Chen and Can Feng

Volume 23, Issue 1, 2022

Published on: 09 December, 2021

Page: [26 - 40] Pages: 15

DOI: 10.2174/1389202922666211110100017

Price: $65

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Abstract

Background: Seed abortion is a common phenomenon in Chinese jujube that seriously hinders the process of cross-breeding. However, the molecular mechanisms of seed abortion remain unclear in jujube.

Methods: Here, we performed transcriptome sequencing using eight flower and fruit tissues at different developmental stages in Ziziphus jujuba Mill. ‘Zhongqiusucui’ to identify key genes related to seed abortion. Histological analysis revealed a critical developmental process of embryo abortion after fertilization.

Results: Comparisons of gene expression revealed a total of 14,012 differentially expressed genes. Functional enrichment analyses of differentially expressed genes between various sample types uncovered several important biological processes, such as embryo development, cellular metabolism, and stress response, that were potentially involved in the regulation of seed abortion. Furthermore, gene co-expression network analysis revealed a suite of potential key genes related to ovule and seed development. We focused on three types of candidate genes, agamous subfamily genes, plant ATP-binding cassette subfamily G transporters, and metacaspase enzymes, and showed that the expression profiles of some members were associated with embryo abortion.

Conclusion: This work generates a comprehensive gene expression data source for unraveling the molecular mechanisms of seed abortion and aids future cross-breeding efforts in jujube.

Keywords: Ziziphus jujuba Mill, seed abortion, embryo abortion, transcriptome, candidate genes, breeding.

Graphical Abstract

[1]
Li, J.W.; Fan, L.P.; Ding, S.D.; Ding, X.L. Nutritional composition of five cultivars of Chinese jujube. Food Chem., 2007, 103(2), 454-460.
[http://dx.doi.org/10.1016/j.foodchem.2006.08.016]
[2]
Liu, M.J. The present status, problems and countermeasures of Chinese jujube production. Rev. China Agric. Sci. Technol., 2000, 2, 76-80.
[3]
Gao, Q.H.; Wu, C.S.; Wang, M. The jujube (Ziziphus jujuba Mill.) fruit: A review of current knowledge of fruit composition and health benefits. J. Agric. Food Chem., 2013, 61(14), 3351-3363.
[http://dx.doi.org/10.1021/jf4007032] [PMID: 23480594]
[4]
Liu, M.J.; Wang, J.R.; Liu, P.; Zhao, J.; Zhao, Z.H.; Dai, L.; Li, X.S.; Liu, Z.G. Historical achievements and frontier advances in the production and research of Chinese jujube (Ziziphus jujuba) in China. Yuan Yi Xue Bao, 2015, 42(9), 1683-1698.
[5]
Qu, Z.Z.; Wang, Y.H. China fruit’s monograph-Chinese jujube volume; For. Publ. House: Beijing, China, 1993, 56, p. 229.
[6]
Liu, M.J.; Wang, J.R.; Liu, P.; Lin, M.J.; Xiao, J.; Liu, Z.G.; Sun, X.C. Design and practice of emasculation-free cross breeding in Chinese jujube. Acta Hortic. Sin., 2014, 41(7), 1495-1502.
[7]
McElver, J.; Tzafrir, I.; Aux, G.; Rogers, R.; Ashby, C.; Smith, K.; Thomas, C.; Schetter, A.; Zhou, Q.; Cushman, M.A.; Tossberg, J.; Nickle, T.; Levin, J.Z.; Law, M.; Meinke, D.; Patton, D. Insertional mutagenesis of genes required for seed development in Arabidopsis thaliana. Genetics, 2001, 159(4), 1751-1763.
[http://dx.doi.org/10.1093/genetics/159.4.1751] [PMID: 11779812]
[8]
Tzafrir, I.; Pena-Muralla, R.; Dickerman, A.; Berg, M.; Rogers, R.; Hutchens, S.; Sweeney, T.C.; McElver, J.; Aux, G.; Patton, D.; Meinke, D. Identification of genes required for embryo development in Arabidopsis. Plant Physiol., 2004, 135(3), 1206-1220.
[http://dx.doi.org/10.1104/pp.104.045179] [PMID: 15266054]
[9]
Ruan, Y.L.; Patrick, J.W.; Bouzayen, M.; Osorio, S.; Fernie, A.R. Molecular regulation of seed and fruit set. Trends Plant Sci., 2012, 17(11), 656-665.
[http://dx.doi.org/10.1016/j.tplants.2012.06.005] [PMID: 22776090]
[10]
McLaughlin, J.E.; Boyer, J.S. Glucose localization in maize ovaries when kernel number decreases at low water potential and sucrose is fed to the stems. Ann. Bot. (Lond.), 2004, 94(1), 75-86.
[http://dx.doi.org/10.1093/aob/mch123] [PMID: 15159218]
[11]
Jin, Y.; Ni, D.A.; Ruan, Y.L. Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell, 2009, 21(7), 2072-2089.
[http://dx.doi.org/10.1105/tpc.108.063719] [PMID: 19574437]
[12]
Mejía, N.; Soto, B.; Guerrero, M.; Casanueva, X.; Houel, C.; Miccono, Mde.L.; Ramos, R.; Le Cunff, L.; Boursiquot, J.M.; Hinrichsen, P.; Adam-Blondon, A.F. Molecular, genetic and transcriptional evidence for a role of VvAGL11 in stenospermocarpic seedlessness in grapevine. BMC Plant Biol., 2011, 11, 57.
[http://dx.doi.org/10.1186/1471-2229-11-57] [PMID: 21447172]
[13]
Bergamini, C.; Cardone, M.F.; Anaclerio, A.; Perniola, R.; Pichierri, A.; Genghi, R.; Alba, V.; Forleo, L.R.; Caputo, A.R.; Montemurro, C.; Blanco, A.; Antonacci, D. Validation assay of p3_VvAGL11 marker in a wide range of genetic background for early selection of stenospermocarpy in Vitis vinifera L. Mol. Biotechnol., 2013, 54(3), 1021-1030.
[http://dx.doi.org/10.1007/s12033-013-9654-8] [PMID: 23483354]
[14]
Zhang, F.; Wang, Z.; Dong, W.; Sun, C.; Wang, H.; Song, A.; He, L.; Fang, W.; Chen, F.; Teng, N. Transcriptomic and proteomic analysis reveals mechanisms of embryo abortion during chrysanthemum cross breeding. Sci. Rep., 2014, 4, 6536.
[http://dx.doi.org/10.1038/srep06536] [PMID: 25288482]
[15]
Liu, H.; Liu, Y.Z.; Zheng, S.Q.; Jiang, J.M.; Wang, P.; Chen, W. Comparative proteomic analysis of longan (Dimocarpus longan Lour.) seed abortion. Planta, 2010, 231(4), 847-860.
[http://dx.doi.org/10.1007/s00425-009-1093-1] [PMID: 20049611]
[16]
Zhu, W.; Chen, X.; Li, H.; Zhu, F.; Hong, Y.; Varshney, R.K.; Liang, X. Comparative transcriptome analysis of aerial and subterranean pods development provides insights into seed abortion in peanut. Plant Mol. Biol., 2014, 85(4-5), 395-409.
[http://dx.doi.org/10.1007/s11103-014-0193-x] [PMID: 24793121]
[17]
Chen, X.; Zhu, W.; Azam, S.; Li, H.; Zhu, F.; Li, H.; Hong, Y.; Liu, H.; Zhang, E.; Wu, H.; Yu, S.; Zhou, G.; Li, S.; Zhong, N.; Wen, S.; Li, X.; Knapp, S.J.; Ozias-Akins, P.; Varshney, R.K.; Liang, X. Deep sequencing analysis of the transcriptomes of peanut aerial and subterranean young pods identifies candidate genes related to early embryo abortion. Plant Biotechnol. J., 2013, 11(1), 115-127.
[http://dx.doi.org/10.1111/pbi.12018] [PMID: 23130888]
[18]
Liu, L.; Wang, J.R.; Liu, M.J.; Zhou, J.Y. Pollion number and its germination rate of different Chinese jujube cultivars. J. Plant Genetic Res., 2006, 7(3), 338-341.
[19]
Zhang, X.Y.; Peng, S.Q.; Guo, Z.H. Studies on the pollination, fertilization and embryo development of Chinese jujube. Sci. Silva Sin., 2004, 40(5), 210-213.
[20]
Li, D.K.; Xue, X.F.; Wang, Y.K.; Zhao, A.L.; Ren, H.Y.; Sui, C.L.; Shi, M.J.; Du, X.H.; Liang, Q. Observation of embryo development an abortion in Chinese jujube (Ziziphus jujuba Mill.). Acta Agric. Boreali-occidentalis Sinica, 2016, 25, 1379-1385.
[21]
Wang, S.; Xie, B.X.; Zhong, Q.P.; Gu, Z.Y.; Zeng, J.Q.; Zeng, J.X. A new Zizyphus jujuba cultivar ‘Zhongqiusucui’. Yuan Yi Xue Bao, 2009, 36, 771-781.
[22]
Shao, F.X.; Wang, S.; Chen, J.; Hong, R.Y. Megasporogenesis, microsporogenesis, and development of female and male gametophytes of Ziziphus jujuba Mill. ‘Zhongqiusucui’. HortScience, 2019, 54(10), 1686-1693.
[http://dx.doi.org/10.21273/HORTSCI14237-19]
[23]
Qu, Z.Z.; Wang, Y.H.; Zhou, J.Z.; Peng, S.Q.; Qi, X.K.; Cheng, S.Z.; Liu, M.J. Observation on flowering characteristics of Zizyphus jujuba Mill. J. Hebei Agric. Univ., 1989, 12(1), 1-9.
[24]
Zeng, M. Biological Characteristics of Zizyphus jujuba Mill; Science Press: Beijing, China, 1959.
[25]
Li, H.P. Plant Microscopic Technique; For. Publ. House: Beijing, China, 2009.
[26]
Xu, M.T.; He, C.N.; Zhang, X.Z.; Qu, J.P.; Zhang, S.Y.; Xu, R.T. Preparation of hematoxylin dyeing solution and improvement of dyeing method. Chin. J. Clin. Exp. Pathol., 2008, 24, 371-372.
[27]
Bolger, A.; Lohse, M.; Usadel, B. Trimmomatic: A flexible read trimming tool for Illumina NGS data. Bioinformatics, 2014, 30(15), 2114-2120.
[http://dx.doi.org/10.1093/bioinformatics/btu170] [PMID: 24695404]
[28]
Trapnell, C.; Pachter, L.; Salzberg, S.L. TopHat: Discovering splice junctions with RNA-Seq. Bioinformatics, 2009, 25(9), 1105-1111.
[http://dx.doi.org/10.1093/bioinformatics/btp120] [PMID: 19289445]
[29]
Langmead, B. Aligning short sequencing reads with Bowtie. Curr. Protoc. Bioinformatics., 2010, 32(1), 11-7.
[http://dx.doi.org/10.1002/0471250953.bi1107s32]
[30]
Li, B.; Dewey, C.N. RSEM: Accurate transcript quantification from RNA-seq data with or without a reference genome. BMC Bioinformatics, 2011, 12, 323-323.
[http://dx.doi.org/10.1186/1471-2105-12-323] [PMID: 21816040]
[31]
Wang, L.; Feng, Z.; Wang, X.; Wang, X.; Zhang, X. DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics, 2010, 26(1), 136-138.
[http://dx.doi.org/10.1093/bioinformatics/btp612] [PMID: 19855105]
[32]
Langfelder, P.; Horvath, S. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 2008, 9, 559.
[http://dx.doi.org/10.1186/1471-2105-9-559] [PMID: 19114008]
[33]
Zhang, B.; Horvath, S. A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol., 2005, 4(1), e17.
[http://dx.doi.org/10.2202/1544-6115.1128] [PMID: 16646834]
[34]
Colombo, L.; Battaglia, R.; Kater, M.M. Arabidopsis ovule development and its evolutionary conservation. Trends Plant Sci., 2008, 13(8), 444-450.
[http://dx.doi.org/10.1016/j.tplants.2008.04.011] [PMID: 18571972]
[35]
Skinner, D.J.; Hill, T.A.; Gasser, C.S. Regulation of ovule development. Plant Cell, 2004, 16(Suppl.), S32-S45.
[http://dx.doi.org/10.1105/tpc.015933] [PMID: 15131247]
[36]
Sundaresan, V. Control of seed size in plants. Proc. Natl. Acad. Sci. USA, 2005, 102(50), 17887-17888.
[http://dx.doi.org/10.1073/pnas.0509021102] [PMID: 16330781]
[37]
Sun, X.; Shantharaj, D.; Kang, X.; Ni, M. Transcriptional and hormonal signaling control of Arabidopsis seed development. Curr. Opin. Plant Biol., 2010, 13(5), 611-620.
[http://dx.doi.org/10.1016/j.pbi.2010.08.009] [PMID: 20875768]
[38]
Brambilla, V.; Battaglia, R.; Colombo, M.; Masiero, S.; Bencivenga, S.; Kater, M.M.; Colombo, L. Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell, 2007, 19(8), 2544-2556.
[http://dx.doi.org/10.1105/tpc.107.051797] [PMID: 17693535]
[39]
Pinyopich, A.; Ditta, G.S.; Savidge, B.; Liljegren, S.J.; Baumann, E.; Wisman, E.; Yanofsky, M.F. Assessing the redundancy of MADS-box genes during carpel and ovule development. Nature, 2003, 424(6944), 85-88.
[http://dx.doi.org/10.1038/nature01741] [PMID: 12840762]
[40]
Favaro, R.; Pinyopich, A.; Battaglia, R.; Kooiker, M.; Borghi, L.; Ditta, G.; Yanofsky, M.F.; Kater, M.M.; Colombo, L. MADS-box protein complexes control carpel and ovule development in Arabidopsis. Plant Cell, 2003, 15(11), 2603-2611.
[http://dx.doi.org/10.1105/tpc.015123] [PMID: 14555696]
[41]
Shi, D.Q.; Yang, W.C. Ovule development in Arabidopsis: Progress and challenge. Curr. Opin. Plant Biol., 2011, 14(1), 74-80.
[http://dx.doi.org/10.1016/j.pbi.2010.09.001] [PMID: 20884278]
[42]
Saha, G.; Park, J.I.; Jung, H.J.; Ahmed, N.U.; Kayum, M.A.; Chung, M.Y.; Hur, Y.; Cho, Y.G.; Watanabe, M.; Nou, I.S. Genome-wide identification and characterization of MADS-box family genes related to organ development and stress resistance in Brassica rapa. BMC Genomics, 2015, 16, 178.
[http://dx.doi.org/10.1186/s12864-015-1349-z] [PMID: 25881193]
[43]
Dreni, L.; Kater, M.M. MADS reloaded: Evolution of the AGAMOUS subfamily genes. New Phytol., 2014, 201(3), 717-732.
[http://dx.doi.org/10.1111/nph.12555] [PMID: 24164649]
[44]
Wei, X.; Wang, L.; Yu, J.; Zhang, Y.; Li, D.; Zhang, X. Genome-wide identification and analysis of the MADS-box gene family in sesame. Gene, 2015, 569(1), 66-76.
[http://dx.doi.org/10.1016/j.gene.2015.05.018] [PMID: 25967387]
[45]
Andolfo, G.; Ruocco, M.; Di Donato, A.; Frusciante, L.; Lorito, M.; Scala, F.; Ercolano, M.R. Genetic variability and evolutionary diversification of membrane ABC transporters in plants. BMC Plant Biol., 2015, 15, 51.
[http://dx.doi.org/10.1186/s12870-014-0323-2] [PMID: 25850033]
[46]
Jasinski, M.; Banasiak, J.; Radom, M.; Kalitkiewicz, A.; Figlerowicz, M. Full-size ABC transporters from the ABCG subfamily in Medicago truncatula. Mol. Plant Microbe Interact., 2009, 22(8), 921-931.
[http://dx.doi.org/10.1094/MPMI-22-8-0921] [PMID: 19589068]
[47]
Jasinski, M.; Ducos, E.; Martinoia, E.; Boutry, M. The ATP-binding cassette transporters: structure, function, and gene family comparison between rice and Arabidopsis. Plant Physiol., 2003, 131(3), 1169-1177.
[http://dx.doi.org/10.1104/pp.102.014720] [PMID: 12644668]
[48]
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. Plant ABC proteins-a unified nomenclature and updated inventory. Trends Plant Sci., 2008, 13(4), 151-159.
[http://dx.doi.org/10.1016/j.tplants.2008.02.001] [PMID: 18299247]
[49]
Çakır, B.; Kılıçkaya, O. Whole-genome survey of the putative ATP-binding cassette transporter family genes in Vitis vinifera. PLoS One, 2013, 8(11), e78860.
[http://dx.doi.org/10.1371/journal.pone.0078860] [PMID: 24244377]
[50]
Dong, J.P.; Kong, W.W.; Li, B.; Huang, B.L. A brief outline of structure and biochemistry characteristics of plant metacaspases. Anhui Nongye Kexue, 2013, 28, 11253-11254, 11258.
[51]
Suarez, M.F.H.; Filonova, L.; Smertenko, A.; Savenkov, E.I.H.; Clapham, D.; Arnold, S.V.; Zhivotovsky, B.V.; Bozhkov, P. Metacaspase-dependent is essential for PCD in plant embryogenesis. Curr. Biol., 2004, 14, 339-340.
[http://dx.doi.org/10.1016/j.cub.2004.04.019]
[52]
Bozhkov, P.V.; Filonova, L.H.; Suarez, M.F.; Helmersson, A.; Smertenko, A.P.; Zhivotovsky, B.; von Arnold, S. VEIDase is a principal caspase-like activity involved in plant programmed cell death and essential for embryonic pattern formation. Cell Death Differ., 2004, 11(2), 175-182.
[http://dx.doi.org/10.1038/sj.cdd.4401330] [PMID: 14576770]
[53]
Bozhkov, P.V.; Suarez, M.F.; Filonova, L.H.; Daniel, G.; Zamyatnin, A.A., Jr; Rodriguez-Nieto, S.; Zhivotovsky, B.; Smertenko, A. Cysteine protease mcII-Pa executes programmed cell death during plant embryogenesis. Proc. Natl. Acad. Sci. USA, 2005, 102(40), 14463-14468.
[http://dx.doi.org/10.1073/pnas.0506948102] [PMID: 16183741]
[54]
Honma, T.; Goto, K. Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature, 2001, 409(6819), 525-529.
[http://dx.doi.org/10.1038/35054083] [PMID: 11206550]
[55]
Ocarez, N.; Mejía, N. Suppression of the D-class MADS-box AGL11 gene triggers seedlessness in fleshy fruits. Plant Cell Rep., 2016, 35(1), 239-254.
[http://dx.doi.org/10.1007/s00299-015-1882-x] [PMID: 26563346]
[56]
Cui, M.J.; Guo, F.F.; Wang, C.; Jiu, S.T.; Zhu, X.D.; Fang, J.G. Identification and roles of VvAGL11 and VvAGL15 gene in the development process of seedless grape berry induced by gibberellin. J. Nanjing Agric. Univ., 2019, 42(1), 261-269.
[57]
Chen, L.N.; Zhang, J.; Niu, J.; Li, H.X.; Xue, H.; Liu, B.B.; Xia, X.C.; Zhang, F.H.; Zhao, D.G.; Cao, S.Y. Cloning and functional verification of gene PgAGL11 associated with the development of flower organs in pomegranate plant. Acta Hortic. Sin., 2017, 44, 2089-2098.
[58]
Rea, P.A. Plant ATP-binding cassette transporters. Annu. Rev. Plant Biol., 2007, 58, 347-375.
[http://dx.doi.org/10.1146/annurev.arplant.57.032905.105406] [PMID: 17263663]
[59]
Panikashvili, D.; Savaldi-Goldstein, S.; Mandel, T.; Yifhar, T.; Franke, R.B.; Höfer, R.; Schreiber, L.; Chory, J.; Aharoni, A. The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol., 2007, 145(4), 1345-1360.
[http://dx.doi.org/10.1104/pp.107.105676] [PMID: 17951461]
[60]
Luo, B.; Xue, X.Y.; Hu, W.L.; Wang, L.J.; Chen, X.Y. An ABC transporter gene of Arabidopsis thaliana, AtWBC11, is involved in cuticle development and prevention of organ fusion. Plant Cell Physiol., 2007, 48(12), 1790-1802.
[http://dx.doi.org/10.1093/pcp/pcm152] [PMID: 17989085]
[61]
Samuels, L.; Kunst, L.; Jetter, R. Sealing plant surfaces: Cuticular wax formation by epidermal cells. Annu. Rev. Plant Biol., 2008, 59, 683-707.
[http://dx.doi.org/10.1146/annurev.arplant.59.103006.093219] [PMID: 18251711]
[62]
McFarlane, H.E.; Shin, J.J.; Bird, D.A.; Samuels, A.L. Arabidopsis ABCG transporters, which are required for export of diverse cuticular lipids, dimerize in different combinations. Plant Cell, 2010, 22(9), 3066-3075.
[http://dx.doi.org/10.1105/tpc.110.077974] [PMID: 20870961]
[63]
Quilichini, T.D.; Friedmann, M.C.; Samuels, A.L.; Douglas, C.J. ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiol., 2010, 154(2), 678-690.
[http://dx.doi.org/10.1104/pp.110.161968] [PMID: 20732973]
[64]
Liu, B.C. Preliminary analysis of the key genes related to ovule abortion related gene VvABCG20 and active GA metabolism in grape; , 2016.
[65]
Van Hautegem, T.; Waters, A.J.; Goodrich, J.; Nowack, M.K. Only in dying, life: Programmed cell death during plant development. Trends Plant Sci., 2015, 20(2), 102-113.
[http://dx.doi.org/10.1016/j.tplants.2014.10.003] [PMID: 25457111]
[66]
Sun, K.; Hunt, K.; Hauser, B.A. Ovule abortion in Arabidopsis triggered by stress. Plant Physiol., 2004, 135(4), 2358-2367.
[http://dx.doi.org/10.1104/pp.104.043091] [PMID: 15299130]
[67]
Zhang, C.; Gong, P.; Wei, R.; Li, S.; Zhang, X.; Yu, Y.; Wang, Y. The metacaspase gene family of Vitis vinifera L.: Characterization and differential expression during ovule abortion in stenospermocarpic seedless grapes. Gene, 2013, 528(2), 267-276.
[http://dx.doi.org/10.1016/j.gene.2013.06.062] [PMID: 23845786]

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