AJPS  Vol.10 No.8 , August 2019
Polyploid Gene Expression and Regulation in Polysomic Polyploids
Abstract: Polyploidization is one of the most crucial pathways in introducing speciation and broadening biodiversity, especially in the Plant Kingdom. Although the majority of studies have focused only on allopolyploid or disomic polyploids, polysomic polyploid species have occurred frequently in higher plants. Due to the occurrence of the capabilities of more copies of alleles in a locus which can have additive dosage effects and/or allelic interactions, polysomic polyploids can lead to unique gene regulations to silence or adjust the expression level to create variations in organ size, metabolic products, and abiotic stress tolerance and biotic stress resistance, etc. This review aims to comprehensively summarize the contemporary understanding and findings concerning the molecular mechanisms of gene expression as well as gene regulation in natural typed and resynthesized polysomic polyploid plants. The review investigates the molecular level of phenomena in polysomic polyploid plants such as 1) typically enlarging organ size and stabilizing meiosis, 2) increasing phytochemical content and metabolic products, 3) enhancing the ability to adapt with biotic and abiotic stress, and 4) changing in gene regulation to silence or adjust the expression levels involve in sequence elimination, methylation, gene suppression, subfunctionalization, neo-functionalization, and transposon activation.
Cite this paper: Van Hieu, P. (2019) Polyploid Gene Expression and Regulation in Polysomic Polyploids. American Journal of Plant Sciences, 10, 1409-1443. doi: 10.4236/ajps.2019.108101.

[1]   Lutz, A.M. (1907) A Prelimiary Note on the Chromosomes of Cenothera lamarckiana and One of Its Mutants, O. Gigas. Science, 26, 151-152.

[2]   Winge, O. (1917) The Chromosome. Their Numbers and General Importance. Comptes-rendus des travaux du Laboratoire Carlsberg, 13, 131-175.

[3]   Kihara, H. and Ono, T. (1926) Chromosomenzahlen und Systematische Gruppierung der Rumex-Arten. Zeitschrift für Zellforschung und Mikroskopische Anatomie, 4, 475-481.

[4]   Buxton, B.H. and Darlington, C.D. (1931) Behaviour of a New Species, Digitalis Mertonensis. Nature, 127, 94.

[5]   Karpechenko, G.D. (1927) The Production of Polyploid Gametes in Hybrids. Hereditas, 9, 349-368.

[6]   Müntzing, A. (1932) Cyto-Genetic Investigation on Synthetic Galeopsis tetrahit. Hereditas, 16, 105-154.

[7]   Osborn, T.C., Pires, J.C., Birchler, J.A., Auger, D.L., Chen, Z.J., Lee, H.S., Comai, L., Madlung, A., Doerge, R.W., Colot, V. and Martienssen, R.A. (2003) Understanding Mechanisms of Novel Gene Expression in Polyploids. Trends in Genetics, 19, 141-147.

[8]   Key, J.M. (1970) Significance of Mating Systems for Chromosomes and Gametes in Polyploids. Hereditas, 66, 165-176.

[9]   Stebbins, G.L. (1947) Types of Polyploids: Their Classification and Significance. Advances in Genetics, 1, 403-429.

[10]   Butruille, D.V. and Boiteux, L.S. (2000) Selection-Mutation Balance in Polysomic Tetraploids: Impact of Double Reduction and Gametophytic Selection on the Frequency and Subchromosomal Localization of Deleterious Mutations. Proceedings of the National Academy of Sciences of the United States of America, 97, 6608-6613.

[11]   Lloyd, A. and Bomblies, K. (2016) Meiosis in Autopolyploid and Allopolyploid Arabidopsis. Current Opinion in Plant Biology, 30, 116-122.

[12]   Lu, Y., Yang, X., Tong, C., Li, X., Feng, S., Wang, Z., Pang, X., Wang, Y., Wang, N., Tobias, C.M. and Wu, R. (2013) A Multivalent Three-Point Linkage Analysis Model of Autotetraploids. Briefings in Bioinformatics, 14, 460-468.

[13]   Barker, M.S., Husband, B.C. and Pires, J.C. (2016) Spreading Winge and Flying High: The Evolutionary Importance of Polyploidy after a Century of Study. American Journal of Botany, 103, 1139-1145.

[14]   Soltis, D.E., Segovia-Salcedo, M.C., Jordon-Thaden, I., Majure, L., Miles, N.M., Mavrodiev, E.V., Mei, W., Cortez, M.B., Soltis,S. and Gitzendanner, M.A. (2014) Are Polyploids Really Evolutionary Dead-Ends (again)? A Critical Reappraisal of Mayrose et al. (2011). The New Phytologist, 202, 1105-1117.

[15]   Mayrose, I., Zhan, S.H., Rothfels, C.J., Arrigo, N., Barker, M.S., Rieseberg, L.H. and Otto, S.P. (2015) Methods for Studying Polyploid Diversification and the Dead End Hypothesis: A Reply to Soltis et al. (2014). New Phytologist, 206, 27-35.

[16]   Spoelhof, J.P., Soltis, S. and Soltis, D.E. (2017) Pure Polyploidy: Closing the Gaps in Autopolyploid Research. Journal of Systematics and Evolution, 55, 340-352.

[17]   Barker, M.S., Arrigo, N., Baniaga, A.E., Li, Z. and Levin, D.A. (2016) On the Relative Abundance of Autopolyploids and Allopolyploids. New phytologist, 210, 391-398.

[18]   Watanabe, K. (2015) Potato Genetics, Genomics and Applications. Breeding Science, 65, 53-68.

[19]   Luo, Z.W., Zhang, Z., Zhang, R.M., Pandey, M., Gailing, O., Hattemer, H.H. and Finkeldey, R. (2006) Modeling Population Genetic Data in Autotetraploid Species. Genetics, 172, 639-646.

[20]   Soltis, S. and Soltis, D.E. (2000) The Role of Genetic and Genomic Attributes in the Success of Polyploids. Proceedings of the National Academy of Sciences of the United States of America, 97, 7051-7057.

[21]   Salman-Minkov, A., Sabath, N. and Mayrose, I. (2016) Whole-Genome Duplication as a Key Factor in Crop Domestication. Nature Plants, 2, Article No. 16115.

[22]   Mammadov, J., Buyyarapu, R., Guttikonda, S.K., Parliament, K., Abdurakhmonov, I.Y. and Kumpatla, S.P. (2018) Wild Relatives of Maize, Rice, Cotton and Soybean: Treasure Troves for Tolerance to Biotic and Abiotic Stresses. Frontiers in Plant Science, 9, 886.

[23]   Machida-Hirano, R. (2015) Diversity of Potato Genetic Resources. Breeding Science, 65, 26-40.

[24]   Bethke, P.C., Halterman, D. and Jansky, S. (2017) Are We Getting Better at Using Wild Potato Species in Light of New Tools? Crop Science, 57, 1241-1258.

[25]   Flint-Garcia, S.A. (2013) Genetics and Consequences of Crop Domestication. Journal of Agricultural and Food Chemistry, 61, 8267-8276.

[26]   Hancock, J.F. (2005) Contributions of Domesticated Plant Studies to our Understanding of Plant Evolution. Annals of Botany, 96, 953-963.

[27]   Vaughan, D.A., Balázs, E. and Heslop-Harrison, J.S. (2007) From Crop Domestication to Super-Domestication. Annals of Botany, 100, 893-901.

[28]   Dar, J., Beigh, Z. and Wani, A.A. (2017) Polyploidy: Evolution and Crop Improvement. In: Bhat, T. and Wani, A., Eds., Chromosome Structure and Aberrations, Springer, New Delhi, 201-218.

[29]   Soltis, D.E., Albert, V.A., Leebens-Mack, J., Bell, C.D., Paterson, A.H., Zheng, C., Sankoff, D., Depamphilis, C.W., Wall, K. and Soltis, S. (2009) Polyploidy and Angiosperm Diversification. American Journal of Botany, 96, 336-348.

[30]   Jiao, Y., Wickett, N.J., Ayyampalayam, S., Chanderbali, A.S., Landherr, L., Ralph, E., Tomsho, L.P., Hu, Y., Liang, H., Soltis, S., Soltis, D.E., Clifton, S.W., Schlarbaum, S.E., Schuster, S.C., Ma, H., Leebens-Mack, J. and dePamphilis, C.W. (2011) Ancestral Polyploidy in Seed Plants and Angiosperms. Nature, 473, 97-100.

[31]   Parisod, C., Holderegger, R. and Brochmann, C. (2010) Evolutionary Consequences of Autopolyploidy. New Phytologist, 186, 5-17.

[32]   Van de Peer, Y., Mizrachi, E. and Marchal, K. (2017) The Evolutionary Significance of Polyploidy. Nature Reviews Genetics, 18, 411-424.

[33]   Drunen, W. and Husband, B.C. (2018) Immediate vs. Evolutionary Consequences of Polyploidy on Clonal Reproduction in an Autopolyploid Plant. Annals of Botany, 122, 195-205.

[34]   Jiao, Y. (2018) Double the Genome, Double the Fun: Genome Duplications in Angiosperms. New Phytologist, 11, 357-358.

[35]   Miller, M., Zhang, C. and Chen, Z.J. (2012) Ploidy and Hybridity Effects on Growth Vigor and Gene Expression in Arabidopsis thaliana Hybrids and Their Parents. G3: Genes, Genomes, Genetics, 2, 505-513.

[36]   Novikova, Y., Hohmann, N. and Van de Peer, Y. (2018) Polyploid Arabidopsis Species Originated around Recent Glaciation Maxima. Current Opinion in Plant Biology, 42, 8-15.

[37]   Soltis, S. and Soltis, D.E. (2016) Ancient WGD Events as Drivers of Key Innovations in Angiosperms. Current Opinion in Plant Biology, 30, 159-165.

[38]   Semon, M. and Wolfe, K.H. (2007) Consequences of Genome Duplication. Current Opinion in Genetics & Development, 17, 505-512.

[39]   Albuzio, A., Spettoli, P. and Cacco, G. (1978) Changes in Gene Expression from Diploid to Autotetraploid Status of Lycopersicum esculentum. Physiologia Plantarum, 44, 77-80.

[40]   Chung, H.H., Shi, S.K., Huang, B. and Chen, J.T. (2017) Enhanced Agronomic Traits and Medicinal Constituents of Autotetraploids in Anoectochilus formosanus Hayata, a Top-Grade Medicinal Orchid. Molecules, 22, 1907.

[41]   Dou, J., Yuan, P.-L., Zhao, S., He, N., Zhu, H., Gao, L., Ji, W., Lu, X. and Liu, W. (2017) Effect of Ploidy Level on Expression of Lycopene Biosynthesis Genes and Accumulation of Phytohormones during Watermelon (Citrullus lanatus) Fruit Development and Ripening. Journal of Integrative Agriculture, 16, 1956-1967.

[42]   Javadian, N., Karimzadeh, G., Sharifi, M., Moieni, A. and Behmanesh, M. (2017) In Vitro Polyploidy Induction: Changes in Morphology, Podophyllotoxin Biosynthesis and Expression of the Related Genes in Linum album (Linaceae). Planta, 245, 1165-1178.

[43]   Mishra, B.K., Pathak, S., Sharma, A., Trivedi, K. and Shukla, S. (2010) Modulated Gene Expression in Newly Synthesized Auto-Tetraploid of Papaver somniferum L. South African Journal of Botany, 76, 447-452.

[44]   Saminathan, T., Nimmakayala,, Manohar, S., Malkaram, S., Almeida, A., Cantrell, R., Tomason, Y., Abburi, L., Rahman, M.A., Vajja, V.G., Khachane, A., Kumar, B., Rajasimha, H.K., Levi, A., Wehner, T. and Reddy, U.K. (2015) Differential Gene Expression and Alternative Splicing between Diploid and Tetraploid Watermelon. Journal of Experimental Botany, 66, 1369-1385.

[45]   De Smet, R., Sabaghian, E., Li, Z., Saeys, Y. and Van de Peer, Y. (2017) Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana. The Plant Cell, 29, 2786-2800.

[46]   Zhou, Y., Kang, L., Liao, S., Pan, Q., Ge, X. and Li, Z. (2015) Transcriptomic Analysis Reveals Differential Gene Expressions for Cell Growth and Functional Secondary Metabolites in Induced Autotetraploid of Chinese Woad (Isatis indigotica Fort.). PLoS ONE, 10, e0116392.

[47]   Martelotto, L.G., Ortiz, J.P.A., Stein, J., Espinoza, F., Quarin, C.L. and Pessino, S.C. (2005) A Comprehensive Analysis of Gene Expression Alterations in a Newly Synthesized Paspalum notatum Autotetraploid. Plant Science, 169, 211-220.

[48]   Lu, B., Ding, R., Zhang, L., Yu, X., Huang, B. and Chen, W. (2006) Molecular Cloning and Characterization of a Novel Calcium-Dependent Protein Kinase Gene IiCPK2 Responsive to Polyploidy from Tetraploid Isatis Indigotica. Journal of Biochemistry and Molecular Biology, 39, 607-617.

[49]   Lu, B., Pan, X., Zhang, L., Huang, B., Sun, L., Li, B., Yi, B., Zheng, S., Yu, X., Ding, R. and Chen, W. (2006) A Genome-Wide Comparison of Genes Responsive to Autopolyploidy in Isatis indigotica Using Arabidopsis thaliana Affymetrix Genechips. Plant Molecular Biology Reporter, 24, 197-204.

[50]   Liu, B. and Sun, G. (2017) MicroRNAs Contribute to Enhanced Salt Adaptation of the Autopolyploid Hordeum bulbosum Compared with Its Diploid Ancestor. The Plant Journal, 91, 57-69.

[51]   Mu, H., Liu, Z., Lin, L., Li, H., Jiang, J. and Liu, G. (2012) Transcriptomic Analysis of Phenotypic Changes in Birch (Betula platyphylla) Autotetraploids. International Journal of Molecular Sciences, 13, 13012-13029.

[52]   Zhang, X., Deng, M. and Fan, G. (2014) Differential Transcriptome Analysis between Paulownia fortunei and Its Synthesized Autopolyploid. International Journal of Molecular Sciences, 15, 5079-5093.

[53]   Zhao, Z., Li, Y., Liu, H., Zhai, X., Deng, M., Dong, Y. and Fan, G. (2017) Genome-Wide Expression Analysis of Salt-Stressed Diploid and Autotetraploid Paulownia tomentosa. PLoS ONE, 12, e0185455.

[54]   Cao, X., Fan, G., Cao, L., Deng, M., Zhao, Z., Niu, S., Wang, Z. and Wang, Y. (2017) Drought Stress-Induced Changes of MicroRNAs in Diploid and Autotetraploid Paulownia tomentosa. Genes & Genomics, 39, 77-86.

[55]   Niu, S., Wang, Y., Zhao, Z., Deng, M., Cao, L., Yang, L. and Fan, G. (2016) Transcriptome and Degradome of MicroRNAs and Their Targets in Response to Drought Stress in the Plants of a Diploid and Its Autotetraploid Paulownia australis. PLoS ONE, 11, e0158750.

[56]   Zhao, Z., Niu, S., Fan, G., Deng, M. and Wang, Y. (2018) Genome-Wide Analysis of Gene and MicroRNA Expression in Diploid and Autotetraploid Paulownia fortunei (Seem) Hemsl. under Drought Stress by Transcriptome, MicroRNA and Degradome Sequencing. Forests, 9, 88.

[57]   Dai, F., Wang, Z., Luo, G. and Tang, C. (2015) Phenotypic and Transcriptomic Analyses of Autotetraploid and Diploid Mulberry (Morus alba L.). International Journal of Molecular Sciences, 16, 22938-22956.

[58]   Xue, H., Zhang, F., Zhang, Z.-H., Fu, J.-F., Wang, F., Zhang, B. and Ma, Y. (2015) Differences in Salt Tolerance between Diploid and Autotetraploid Apple Seedlings Exposed to Salt Stress. Scientia Horticulturae, 190, 24-30.

[59]   Pegoraro, L., Cafasso, D., Rinaldi, R., Cozzolino, S. and Scopece, G. (2016) Habitat Preference and Flowering-Time Variation Contribute to Reproductive Isolation Between Diploid and Autotetraploid Anacamptis pyramidalis. Journal of Evolutionary Biology, 29, 2070-2082.

[60]   Münzbergová, Z. and Skuhrovec, J. (2017) Contrasting Effects of Ploidy Level on Seed Production in a Diploid-Tetraploid System. AoB Plants, 9, plw077.

[61]   Hollister, J.D., Arnold, B.J., Svedin, E., Xue, K.S., Dilkes, B.P. and Bomblies, K. (2012) Genetic Adaptation Associated with Genome-Doubling in Autotetraploid Arabidopsis arenosa. PLoS Genetics, 8, e1003093.

[62]   Rastogi, S. and Liberles, D.A. (2005) Subfunctionalization of Duplicated Genes as a Transition State to Neofunctionalization. BMC Evolutionary Biology, 5, 28.

[63]   Conant, G.C. and Wolfe, K.H. (2008) Turning a Hobby into a Job: How Duplicated Genes Find New Functions. Nature Reviews Genetics, 9, 938-950.

[64]   Gu, A.X., Zhao, J.J., Li, L.M., Wang, Y.H., Zhao, Y.J., Hua, F., Xu, Y.C. and Shen, S.X. (2016) Analyses of Phenotype and ARGOS and ASY1 Expression in a Ploidy Chinese Cabbage Series Derived from One Haploid. Breeding Science, 66, 161-168.

[65]   Halterman, D., Guenthner, J., Collinge, S., Butler, N. and Douches, D. (2016) Biotech Potatoes in the 21st Century: 20 Years Since the First Biotech Potato. American Journal of Potato Research, 93, 1-20.

[66]   Wang, B., Sang, Y., Song, J., Gao, X.Q. and Zhang, X. (2009) Expression of a Rice OsARGOS Gene in Arabidopsis Promotes Cell Division and Expansion and Increases Organ Size. Journal of Genetics and Genomics 36, 31-40.

[67]   Bird, D., Beisson, F., Brigham, A., Shin, J., Greer, S., Jetter, R., Kunst, L., Wu, X., Yephremov, A. and 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.

[68]   Narukawa, H., Yokoyama, R., Komaki, S., Sugimoto, K. and Nishitani, K. (2015) Stimulation of Cell Elongation by Tetraploidy in Hypocotyls of Dark-Grown Arabidopsis Seedlings. PLoS ONE, 10, e0134547.

[69]   Narukawa, H., Yokoyama, R. and Nishitani, K. (2016) Possible Pathways Linking Ploidy Level to Cell Elongation and Cuticular Function in Hypocotyls of Dark-Grown Arabidopsis Seedlings. Plant Signaling & Behavior, 11, e1118597.

[70]   Corneillie, S., De Storme, N., Van Acker, R., Fangel, J.U., De Bruyne, M., De Rycke, R., Geelen, D., Willats, W.G.T., Vanholme, B. and Boerjan, W. (2019) Polyploidy Affects Plant Growth and Alters Cell Wall Composition. Plant Physiology, 179, 74-87.

[71]   Alam, H., Razaq, M. and Salahuddin (2015) Induced Polyploidy as a Tool for Increasing Tea (Camellia sinensis L.) Production. Journal of Northeast Agricultural University, 22, 43-47.

[72]   Ma, Y., Xue, H., Zhang, L., Zhang, F., Ou, C., Wang, F. and Zhang, Z. (2016) Involvement of Auxin and Brassinosteroid in Dwarfism of Autotetraploid Apple (Malus×domestica). Scientific Reports, 6, 26719.

[73]   Allario, T., Brumos, J., Colmenero-Flores, J.M., Tadeo, F., Froelicher, Y., Talon, M., Navarro, L., Ollitrault, P. and Morillon, R. (2011) Large Changes in Anatomy and Physiology between Diploid Rangpur Lime (Citrus limonia) and Its Autotetraploid Are Not Associated with Large Changes in Leaf Gene Expression. Journal of Experimental Botany, 62, 2507-2519.

[74]   Wang, Z., Fan, G., Dong, Y., Zhai, X., Deng, M., Zhao, Z., Liu, W. and Cao, Y. (2017) Implications of Polyploidy Events on the Phenotype, Microstructure and Proteome of Paulownia australis. PLoS ONE, 12, e0172633.

[75]   Pelé, A., Rousseau-Gueutin, M. and Chèvre, A.-M. (2018) Speciation Success of Polyploid Plants Closely Relates to the Regulation of Meiotic Recombination. Frontiers in Plant Science, 9, 907.

[76]   Wu, J., Shahid, M.Q., Guo, H., Yin, W., Chen, Z., Wang, L., Liu, X. and Lu, Y. (2014) Comparative Cytological and Transcriptomic Analysis of Pollen Development in Autotetraploid and Diploid Rice. Plant Reproduction, 27, 181-196.

[77]   Wright, K.M., Arnold, B., Xue, K., Surinová, M., O’Connell, J. and Bomblies, K. (2015) Selection on Meiosis Genes in Diploid and Tetraploid Arabidopsis arenosa. Molecular Biology and Evolution, 32, 944-955.

[78]   Da Ines, O., Degroote, F., Goubely, C., Amiard, S., Gallego, M.E. and White, C.I. (2013) Meiotic Recombination in Arabidopsis Is Catalysed by DMC1, with RAD51 Playing a Supporting Role. PLoS Genetics, 9, e1003787.

[79]   Braynen, J., Yang, Y., Wei, F., Cao, G., Shi, G., Tian, B., Zhang, X., Jia, H., Wei, X. and Wei, Z. (2017) Transcriptome Analysis of Floral Buds Deciphered an Irregular Course of Meiosis in Polyploid Brassica rapa. Front Plant Science, 8, 768.

[80]   Li, X., Shahid, M.Q., Xia, J., Lu, Z., Fang, N., Wang, L., Wu, J., Chen, Z. and Liu, X. (2017) Analysis of Small RNAs Revealed Differential Expressions during Pollen and Embryo Sac Development in Autotetraploid Rice. BMC Genomics, 18, 129.

[81]   Liu, W., Zhao, S., Cheng, Z., Wan, X., Yan, Z. and King, S.R. (2010) Lycopene and Citrulline Contents in Watermelon (Citrullus lanatus) Fruit with Different Ploidy and Changes during Fruit Development. Acta Horticulturae, 871, 543-550.

[82]   Zhao, W., Lv, P. and Gu, H. (2013) Studies on Carotenoids in Watermelon Flesh. Agricultural Sciences, 4, 13-20.

[83]   Vergara, F., Kikuchi, J. and Breuer, C. (2016) Artificial Autopolyploidization Modifies the Tricarboxylic Acid Cycle and GABA Shunt in Arabidopsis thaliana Col-0. Scientific Reports, 6, 26515.

[84]   Preet, R. and Gupta, R.C. (2017) Fatty Acid Profiling in Diploid (n = 12) and Tetraploid Cytotypes (n = 24) of Physalis angulata LINN from Rajasthan by Gas Chromatography International Journal of Pharmaceutical Sciences and Research, 8, 3458-3462.

[85]   Tu, Y., Jiang, A., Gan, L., Hossain, M., Zhang, J., Peng, B., Xiong, Y., Song, Z., Cai, D., Xu, W., Zhang, J. and He, Y. (2014) Genome Duplication Improves Rice Root Resistance to Salt Stress. Rice, 7, 15.

[86]   Visger, C., Wong, G.K.S., Zhang, Y., Soltis, S. and Soltis, D.E. (2017) Divergent Gene Expression Levels between Diploid and Autotetraploid Tolmiea (Saxifragaceae) Relative to the Total Transcriptome, the Cell and Biomass. BioRxiv, 1-35.

[87]   Fan, G., Wang, L., Deng, M., Niu, S., Zhao, Z., Xu, E., Cao, X. and Zhang, X. (2015) Transcriptome Analysis of the Variations between Autotetraploid Paulownia tomentosa and Its Diploid Using High-Throughput Sequencing. Molecular Genetics and Genomics, 290, 1627-1638.

[88]   Fasano, C., Diretto, G., Aversano, R., D’Agostino, N., Di Matteo, A., Frusciante, L., Giuliano, G. and Carputo, D. (2016) Transcriptome and Metabolome of Synthetic Solanum Autotetraploids Reveal Key Genomic Stress Events Following Polyploidization. New Phytologist, 210, 1382-1394.

[89]   Tsukaya, H., Sawada, Y., Oikawa, A., Shiratake, K., Isuzugawa, K., Saito, K. and Hirai, M.Y. (2015) Intraspecific Comparative Analyses of Metabolites between Diploid and Tetraploid Arabidopsis thaliana and Pyrus communis. New Negatives in Plant Science, 1-2, 53-61.

[90]   Vergara, F., Rymen, B., Kuwahara, A., Sawada, Y., Sato, M. and Hirai, M.Y. (2017) Autopolyploidization, Geographic Origin and Metabolome Evolution in Arabidopsis thaliana. American Journal of Botany, 104, 905-914.

[91]   Yan, K., Wu, C., Zhang, L. and Chen, X. (2015) Contrasting Photosynthesis and Photoinhibition in Tetraploid and Its Autodiploid Honeysuckle (Lonicera japonica Thunb.) under Salt Stress. Frontiers in Plant Science, 6, 227.

[92]   Meng, H., Jiang, S., Hua, S., Lin, X., Li, Y., Guo, W. and Jiang, L. (2011) Comparison between a Tetraploid Turnip and Its Diploid Progenitor (Brassica rapa L.): The Adaptation to Salinity Stress. Agricultural Sciences in China, 10, 363-375.

[93]   Yu, L., Liu, X., Boge, W. and Liu, X. (2016) Genome-Wide Association Study Identifies Loci for Salt Tolerance during Germination in Autotetraploid Alfalfa (Medicago sativa L.) Using Genotyping-by-Sequencing. Frontiers in Plant Science, 7, 956.

[94]   Chao, D.Y., Dilkes, B., Luo, H., Douglas, A., Yakubova, E., Lahner, B. and Salt, D.E. (2013) Polyploids Exhibit Higher Potassium Uptake and Salinity Tolerance in Arabidopsis. Science, 341, 658-659.

[95]   Fan, G., Li, X., Deng, M., Zhao, Z. and Yang, L. (2016) Comparative Analysis and Identification of miRNAs and Their Target Genes Responsive to Salt Stress in Diploid and Tetraploid Paulownia fortunei Seedlings. PLoS ONE, 11, e0149617.

[96]   Li, M., Xu, G., Xia, X., Wang, M., Yin, X., Zhang, B., Zhang, X. and Cui, Y. (2017) Deciphering the Physiological and Molecular Mechanisms for Copper Tolerance in Autotetraploid Arabidopsis. Plant Cell Reports, 36, 1585-1597.

[97]   Zhang, X.Y., Hu, C.G. and Yao, J.L. (2010) Tetraploidization of Diploid Dioscorea Results in Activation of the Antioxidant Defense System and Increased Heat Tolerance. Journal of Plant Physiology, 167, 88-94.

[98]   Mu, H., Lin, L., Zhang, Q., Tang, X., Zhang, X. and Cheng, G. (2016) Growth, Proline Content and Proline-Associated Gene Expression of Autotetraploid Betula platyphylla Responding to NaHCO3 Stress. Dendrobiology, 75, 123-129.

[99]   El-Morsy, S., Dorra, D.M.M., El-Hady, A., Hiaba, A.A.A. and Mohamed, Y.A. (2009) Comparative Studies on Diploid and Tetraploid Levels of Nicotiana alata. Academic Journal of Plant Sciences, 2, 182-188.

[100]   Ruiz, M., Quinones, A., Martínez-Alcántara, B., Aleza, P., Morillon, R., Navarro, L., Primo-Millo, E. and Martínez-Cuenca, M. (2016) Tetraploidy Enhances Boron-Excess Tolerance in Carrizo Citrange (Citrus sinensis L. Osb. × Poncirus trifoliata L. Raf.). Frontiers in Plant Science, 7, 701.

[101]   Yan, L., Fan, G., Deng, M., Zhao, Z., Dong, Y. and Li, Y. (2017) Comparative Proteomic Analysis of Autotetraploid and Diploid Paulownia tomentosa Reveals Proteins Associated with Superior Photosynthetic Characteristics and Stress Adaptability in Autotetraploid Paulownia. Physiology and Molecular Biology of Plants, 23, 605-617.

[102]   Deng, M., Dong, Y., Zhao, Z., Li, Y. and Fan, G. (2017) Dissecting the Proteome Dynamics of the Salt Stress Induced Changes in the Leaf of Diploid and Autotetraploid Paulownia fortunei. PLoS ONE, 12, e0181937.

[103]   del Pozo, J.C. and Ramirez-Parra, E. (2014) Deciphering the Molecular Bases for Drought Tolerance in Arabidopsis Autotetraploids. Plant, Cell & Environment, 37, 2722-2737.

[104]   Deng, B., Du, W., Liu, C., Sun, W., Tian, S. and Dong, H. (2012) Antioxidant Response to Drought, Cold and Nutrient Stress in Two Ploidy Levels of Tobacco Plants: Low Resource Requirement Confers Polytolerance in Polyploids? Plant Growth Regulation, 66, 37-47.

[105]   Hias, N., Svara, A. and Keulemans, J.W. (2018) Effect of Polyploidisation on the Response of Apple (Malus × domestica Borkh.) to Venturia inaequalis Infection. European Journal of Plant Pathology, 151, 515-526.

[106]   Gao, R., Wang, H., Dong, B., Yang, X., Chen, S., Jiang, J., Zhang, Z., Liu, C., Zhao, N. and Chen, F. (2016) Morphological, Genome and Gene Expression Changes in Newly Induced Autopolyploid Chrysanthemum lavandulifolium (Fisch. ex Trautv.) Makino. International Journal of Molecular Sciences, 17, 1690.

[107]   De Smet, R., Adams, K.L., Vandepoele, K., Van Montagu, M.C.E., Maere, S. and Van de Peer, Y. (2013) Convergent Gene Loss Following Gene and Genome Duplications Creates Single-Copy Families in Flowering Plants. Proceedings of the National Academy of Sciences of the United States of America, 110, 2898-2903.

[108]   Stupar, R.M., Bhaskar, B., Yandell, B.S., Rensink, W.A., Hart, A.L., Ouyang, S., Veilleux, R.E., Busse, J.S., Erhardt, R.J., Buell, C.R. and Jiang, J. (2007) Phenotypic and Transcriptomic Changes Associated With Potato Autopolyploidization. Genetics, 176, 2055-2067.

[109]   Zhang, H., Zhao, H., Wu, S., Huang, F., Wu, K., Zeng, X., Chen, X., Xu, and Wu, X. (2016) Global Methylation Patterns and Their Relationship with Gene Expression and Small RNA in Rice Lines with Different Ploidy. Frontiers in Plant Science, 7, 1002.

[110]   Zhang, J., Liu, Y., Xia, E., Yao, Q., Liu, X. and Gao, L. (2015) Autotetraploid Rice Methylome Analysis Reveals Methylation Variation of Transposable Elements and Their Effects on Gene Expression. Proceedings of the National Academy of Sciences of the United States of America, 112, E7022-E7029.

[111]   Lavania, U.C., Srivastava, S., Lavania, S., Basu, S., Misra, N.K. and Mukai, Y. (2012) Autopolyploidy Differentially Influences Body Size in Plants, but Facilitates Enhanced Accumulation of Secondary Metabolites, Causing Increased Cytosine Methylation. Plant Journal, 71, 539-549.

[112]   Church, S.A. and Spaulding, E.J. (2009) Gene Expression in a Wild Autopolyploid Sunflower Series. Journal of Heredity, 100, 491-495.

[113]   Dong, B., Wang, H., Song, A., Liu, T., Chen, Y., Fang, W., Chen, S., Chen, F., Guan, Z. and Jiang, J. (2016) miRNAs Are Involved in Determining the Improved Vigor of Autotetrapoid Chrysanthemum nankingense. Frontiers in Plant Science, 7, 1412.

[114]   Xu, Y., Zhang, W., Chen, G. and Wang, J. (2017) DNA Methylation Alteration Is a Major Consequence of Genome Doubling in Autotetraploid Brassica rapa. Archives of Biological Sciences, 69, 689-697.

[115]   He, P., Cheng, L., Li, H., Wang, H. and Li, L. (2017) A Comparative Analysis of DNA Methylation in Diploid and Tetraploid Apple (Malus × domestica Borkh.). Czech Journal of Genetics and Plant Breeding, 53, 63-68.

[116]   Dar, T.H., Raina, S.N. and Goel, S. (2017) Cytogenetic and Molecular Evidences Revealing Genomic Changes after Autopolyploidization: A Case Study of Synthetic Autotetraploid Phlox drummondii Hook. Physiology and Molecular Biology of Plants, 23, 641-650.

[117]   Liu, S., Yang, Y., Wei, F., Duan, J., Braynen, J., Tian, B., Cao, G., Shi, G. and Yuan, J. (2017) Autopolyploidy Leads to Rapid Genomic Changes in Arabidopsis thaliana. Theory in Biosciences, 136, 199-206.

[118]   Arsovski, A.A. and Pradinuk, J. (2015) Evolution of Cis-Regulatory Elements and Regulatory Networks in Duplicated Genes of Arabidopsis. Plant Physiology, 169, 2982-2991.

[119]   Qiao, G., Liu, M., Song, K., Li, H., Yang, H., Yin, Y. and Zhuo, R. (2017) Phenotypic and Comparative Transcriptome Analysis of Different Ploidy Plants in Dendrocalamus latiflorus Munro. Frontiers in Plant Science, 8, 1371.

[120]   Weiss, H. and Maluszynska, J. (2000) Chromosomal Rearrangement in Autotetraploid Plants of Arabidopsis thaliana. Hereditas, 133, 255-261.

[121]   Mena, M., Ambrose, B., Meeley, R., Briggs, S., Yanofsky, M. and Schmidt, R. (1996) Diversification of C-Function Activity in Maize Flower Development. Science, 274, 1537-1540.

[122]   Hu, C., Lin, S., Chi, W. and Charng, Y. (2012) Recent Gene Duplication and Subfunctionalization Produced a Mitochondrial GrpE, the Nucleotide Exchange Factor of the Hsp70 Complex, Specialized in Thermotolerance to Chronic Heat Stress in Arabidopsis. Plant Physiology, 158, 747-758.

[123]   D’Amelia, V., Aversano, R., Ruggiero, A., Batelli, G., Appelhagen, I., Dinacci, C., Hill, L., Martin, C. and Carputo, D. (2018) Subfunctionalization of Duplicate MYB Genes in Solanum commersonii Generated the Cold-Induced ScAN2 and the Anthocyanin Regulator ScAN1. Plant, Cell & Environment, 41, 1038-1051.

[124]   Drea, S.C., Lao, N.T., Wolfe, K.H. and Kavanagh, T.A. (2006) Gene Duplication, Exon Gain and Neofunctionalization of OEP16-Related Genes in Land Plants. The Plant Journal, 46, 723-735.

[125]   Erdmann, R., Gramzow, L., Melzer, R., Theissen, G. and Becker, A. (2010) GORDITA (AGL63) Is a Young Paralog of the Arabidopsis thaliana Bsister MADS Box Gene ABS (TT16) that Has Undergone Neofunctionalization. The Plant Journal, 63, 914-924.

[126]   Mollinari, M. and Garcia, A.A.F. (2018) Linkage Analysis and Haplotype Phasing in Experimental Autopolyploid Populations with High Ploidy Level Using Hidden Markov Models. BioRxiv, Article ID: 415232.

[127]   Vicient, C.M. and Casacuberta, J.M. (2017) Impact of Transposable Elements on Polyploid Plant Genomes. Annals of Botany, 120, 195-207.

[128]   Bardil, A., Tayale, A. and Parisod, C. (2015) Evolutionary Dynamics of Retrotransposons Following Autopolyploidy in the Buckler Mustard Species Complex. The Plant Journal, 82, 621-631.

[129]   Zhou, K., Fleet, P., Nevo, E., Zhang, X. and Sun, G. (2017) Transcriptome Analysis Reveals Plant Response to Colchicine Treatment during on Chromosome Doubling. Scientific Reports, 7, 8503.

[130]   Ren, R., Wang, H., Guo, C., Zhang, N., Zeng, L., Chen, Y., Ma, H. and Qi, J. (2018) Widespread Whole Genome Duplications Contribute to Genome Complexity and Species Diversity in Angiosperms. Molecular Plant, 11, 414-428.

[131]   Gout, J. and Lynch, M. (2015) Maintenance and Loss of Duplicated Genes by Dosage Subfunctionalization. Molecular Biology and Evolution, 32, 2141-2148.

[132]   Shi, X., Zhang, C., Ko, D.K. and Chen, Z.J. (2015) Genome-Wide Dosage-Dependent and -Independent Regulation Contributes to Gene Expression and Evolutionary Novelty in Plant Polyploids. Molecular Biology and Evolution, 32, 2351-2366.

[133]   Fan, G., Wang, L., Deng, M., Zhao, Z., Dong, Y., Zhang, X. and Li, Y. (2016) Changes in Transcript Related to Osmosis and Intracellular Ion Homeostasis in Paulownia tomentosa under Salt Stress. Frontiers in Plant Science, 7, 384.

[134]   Gavrilenko, T., Thieme, R. and Rokka, V.M. (2001) Cytogenetic Analysis of Lycopersicon Esculentum (+) Solanum etuberosum Somatic Hybrids and Their Androgenetic Regenerants. Theoretical and Applied Genetics, 103, 231-239.

[135]   Guerra, D., Teresa Schifino Wittmann, M., Schwarz, S., Souza, P., Gonzatto, M. and Weiler, R. (2014) Comparison between Diploid and Tetraploid Citrus Rootstocks: Morphological Characterization and Growth Evaluation. Bragantia, 73, 1-7.

[136]   Tang, Z., Chen, D., Song, Z., He, Y. and Cai, D. (2010) In Vitro Induction and Identification of Tetraploid Plants of Paulownia tomentosa. Plant Cell Tissue and Organ Culture, 102, 213-220.

[137]   Balogh, L. (2008) Sunflower species (Helianthus spp.). Institute of Ecology and Botany, Hungarian Academy of Sciences, Vácrátót, Hungary. 227-255.

[138]   Bombarely, A., Rosli, H., Vrebalov, J., Moffett, P., Mueller, L. and Martin, G. (2012) A Draft Genome Sequence of Nicotiana benthamiana to Enhance Molecular Plant-Microbe Biology Research. Molecular Plant-Microbe Interactions, 25, 1523-1530.

[139]   Fan, G.Q., Cao, Y.C., Zhao, Z.L. and Yang, Z.Q. (2007) Induction of Autotetraploid of Paulownia fortunei. Scientia Silvae Sinicae, 43, 31-35.

[140]   Nasr, M., Habib, H.M., Ibrahim, I.A. and Kapiel, T. (2004) In Vitro Induction of Autotetraploid Watermelons Using Colchicine and Four Dinitroaniline Compounds. Proceedings of International Conference of Genetic Engineering and Its Applications, Sharm Elsheik, Egypt, 8-11 April 2004, 1-20.

[141]   Kamm, A., Galasso, I., Schmidt, T. and Heslop-Harrison, J.S. (1995) Analysis of a Repetitive DNA Family from Arabidopsis arenosa and Relationships between Arabidopsis Species. Plant Molecular Biology, 27, 853-862.

[142]   Albayrak, S., Türk, M., SevImay, C.S. and Anakhatoon, E. (2015) Karyotype Characterization of Alfalfa (Medicago sativa L.) Collected from Lake Regions of Turkey. Scientific Papers—Series A, Agronomy, 58, 351-353.

[143]   Li, L., Deng, C.H., Knabel, M., Chagné, D., Kumar, S., Sun, J., Zhang, S. and Wu, J. (2017) Integrated High-Density Consensus Genetic Map of Pyrus and Anchoring of the ‘Bartlett’ v1.0 (Pyrus communis) Genome. DNA Research, 24, 289-301.