Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid
Abstract
:1. Introduction
2. Materials and Methods
2.1. Plant Materials, DNA, and RNA Extraction
2.2. Gene Cloning and Quantitative Real-Time PCR Analysis
2.3. Quantification and Comparison of rbcS Aallelic and Homeologous Expression Based on RNA-Sequencing
2.4. The Prediction of RuBisCO Protein–Protein Complex Binding Affinity
2.5. Measurement of RuBisCO Activity and Content
2.6. Statistical Analysis
3. Results
3.1. Sequence Variation of RuBisCO Encoding Genes in Cucumis Allopolyploid
3.2. Expression of Maternal Inheritance of the rbcL Gene and Duplicated rbcS Genes in Allotetraploid C. × hytivus
3.3. The Prediction of the RuBisCO Protein–Protein Complex Binding Affinity
3.4. The Influence of Allopolyploidization on RuBisCO Content and Activity
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Conflicts of Interest
References
- Leitch, I.J.; Bennett, M.D. Polyploidy in angiosperms. Trends Plant Sci. 1997, 2, 470–476. [Google Scholar] [CrossRef]
- Wendel, J.F. Genome evolution in polyploids. Plant Mol. Biol. 2000, 42, 225–249. [Google Scholar] [CrossRef] [PubMed]
- Soltis, D.E.; Albert, V.A.; Leebens-Mack, J.; Bell, C.D.; Paterson, A.H.; Zheng, C.F.; Sankoff, D.; de Pamphilis, C.W.; Wall, P.K.; Soltis, P.S. Polyploidy and angiosperm diversification. Am. J. Bot. 2009, 96, 336–348. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiao, Y.N.; Wickett, N.J.; Ayyampalayam, S.; Chanderbali, A.S.; Landherr, L.; Ralph, P.E.; Tomsho, L.P.; Hu, Y.; Liang, H.Y.; Soltis, P.S.; et al. Ancestral polyploidy in seed plants and angiosperms. Nature 2011, 473, 97–U113. [Google Scholar] [CrossRef]
- Adams, K.L.; Wendel, J.F. Polyploidy and genome evolution in plants. Curr. Opin. Plant. Biol. 2005, 8, 135–141. [Google Scholar] [CrossRef]
- Lim, K.Y.; Kovarik, A.; Matyasek, R.; Chase, M.W.; Clarkson, J.J.; Grandbastien, M.A.; Leitch, A.R. Sequence of events leading to near-complete genome turnover in allopolyploid Nicotiana within five million years. New Phytol. 2007, 175, 756–763. [Google Scholar] [CrossRef]
- Buggs, R.J.A.; Chamala, S.; Wu, W.; Tate, J.A.; Schnable, P.S.; Soltis, D.E.; Soltis, P.S.; Barbazuk, W.B. Rapid, repeated, and clustered loss of duplicate genes in allopolyploid plant populations of independent origin. Curr. Biol. 2012, 22, 248–252. [Google Scholar] [CrossRef]
- Yu, X.Q.; Wang, X.X.; Hyldgaard, B.; Zhu, Z.B.; Zhou, R.; Kjaer, K.H.; Ouzounis, T.; Lou, Q.F.; Li, J.; Cai, Q.; et al. Allopolyploidization in Cucumis contributes to delayed leaf maturation with repression of redundant homoeologous genes. Plant J. 2018, 94, 393–404. [Google Scholar] [CrossRef]
- Flagel, L.E.; Wendel, J.F. Evolutionary rate variation, genomic dominance and duplicate gene expression evolution during allotetraploid cotton speciation. New Phytol. 2010, 186, 184–193. [Google Scholar] [CrossRef]
- Bottani, S.; Zabet, N.R.; Wendel, J.F.; Veitia, R.A. Gene expression dominance in allopolyploids: Hypotheses and models. Trends Plant Sci. 2018, 23, 393–402. [Google Scholar] [CrossRef]
- Paun, O.; Bateman, R.M.; Fay, M.F.; Hedren, M.; Civeyrel, L.; Chase, M.W. Stable epigenetic effects impact adaptation in allopolyploid orchids (Dactylorhiza: Orchidaceae). Mol. Biol. Evol. 2010, 27, 2465–2473. [Google Scholar] [CrossRef] [PubMed]
- Taylor, W.C. Regulatory interactions between nuclear and plastid genomes. Annu. Rev. Plant Phys. 1989, 40, 211–233. [Google Scholar] [CrossRef]
- Crespi, B.; Nosil, P. Conflictual speciation: Species formation via genomic conflict. Trends Ecol. Evol. 2013, 28, 48–57. [Google Scholar] [CrossRef] [PubMed]
- Campbell, D.R.; Waser, N.M.; Aldridge, G.; Wu, C.A. Lifetime fitness in two generations of ipomopsis hybrids. Evolution 2008, 62, 2616–2627. [Google Scholar] [CrossRef] [PubMed]
- Reboud, X.; Zeyl, C. Organelle inheritance in plants. Heredity 1994, 72, 132–140. [Google Scholar] [CrossRef] [Green Version]
- Wang, T.; Li, Y.; Shi, Y.; Reboud, X.; Darmency, H.; Gressel, J. Low frequency transmission of a plastid-encoded trait in Setaria italica. Theor. Appl. Genet. 2004, 108, 315–320. [Google Scholar] [CrossRef]
- Azhagiri, A.K.; Maliga, P. Exceptional paternal inheritance of plastids in Arabidopsis suggests that low-frequency leakage of plastids via pollen may be universal in plants. Plant J. 2007, 52, 817–823. [Google Scholar] [CrossRef]
- Svab, Z.; Maliga, P. Exceptional transmission of plastids and mitochondria from the transplastomic pollen parent and its impact on transgene containment. Proc. Natl. Acad. Sci. USA 2007, 104, 7003–7008. [Google Scholar] [CrossRef] [Green Version]
- Sharbrough, J.; Conover, J.L.; Tate, J.A.; Wendel, J.F.; Sloan, D.B. Cytonuclear responses to genome doubling. Am. J. Bot 2017, 104, 1277–1280. [Google Scholar] [CrossRef] [Green Version]
- Gong, L.; Olson, M.; Wendel, J.F. Cytonuclear evolution of rubisco in four allopolyploid lineages. Mol. Biol. Evol. 2014, 31, 2624–2636. [Google Scholar] [CrossRef]
- Wang, X.F.; Dong, Q.L.; Li, X.C.; Yuliang, A.Z.; Yu, Y.N.; Li, N.; Liu, B.; Gong, L. cytonuclear variation of rubisco in synthesized rice hybrids and allotetraploids. Plant. Genome Us 2017, 10. [Google Scholar] [CrossRef] [PubMed]
- Ferreira de Carvalho, J.; Lucas, J.; Deniot, G.; Falentin, C.; Filangi, O.; Gilet, M.; Legeai, F.; Lode, M.; Morice, J.; Trotoux, G.; et al. Cytonuclear interactions remain stable during allopolyploid evolution despite repeated whole-genome duplications in Brassica. Plant J. 2019, 98, 434–447. [Google Scholar] [CrossRef] [PubMed]
- Chen, J.F.; Staub, J.E.; Tashiro, Y.; Isshiki, S.; Miyazaki, S. Successful interspecific hybridization between Cucumis sativus L. and C. C-hystrix Chakr. Euphytica 1997, 96, 413–419. [Google Scholar] [CrossRef]
- Chen, J.F.; Kirkbride, J.H. A new synthetic species of Cucumis (Cucurbitaceae) from interspecific hybridization and chromosome doubling. Brittonia 2000, 52, 315–319. [Google Scholar] [CrossRef]
- Havey, M.J.; McCreight, J.D.; Rhodes, B.; Taurick, G. Differential transmission of the Cucumis organellar genomes. Theor Appl Genet. 1998, 97, 122–128. [Google Scholar] [CrossRef]
- Shen, J.; Zhao, J.; Bartoszewski, G.; Malepszy, S.; Havey, M.; Chen, J.F. Persistence and protection of mitochondrial DNA in the generative cell of cucumber is consistent with its paternal transmission. Plant. Cell Physiol 2015, 56, 2271–2282. [Google Scholar] [CrossRef] [PubMed]
- Shen, J.; Kere, M.G.; Chen, J.F. Mitochondrial genome is paternally inherited in Cucumis allotetraploid (C. x hytivus) derived by interspecific hybridization. Sci. Hortic-Amsterdam 2013, 155, 39–42. [Google Scholar] [CrossRef]
- Murraary, M.G.; Thompsom, W.F. Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res. 1980, 8, 4321–4325. [Google Scholar] [CrossRef]
- Gong, L.; Salmon, A.; Yoo, M.J.; Grupp, K.K.; Wang, Z.N.; Paterson, A.H.; Wendel, J.F. The cytonuclear dimension of allopolyploid evolution: An example from cotton using rubisco. Mol. Biol. Evol. 2012, 29, 3023–3036. [Google Scholar] [CrossRef]
- Li, J.; Li, Z.G.; Tang, L.; Yang, Y.W.; Zouine, M.; Bouzayen, M. A conserved phosphorylation site regulates the transcriptional function of ETHYLENE-INSENSITIVE3-like1 in tomato. J. Exp. Bot. 2012, 63, 427–439. [Google Scholar] [CrossRef]
- Livak, K.J.; Schmittgen, T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 2001, 25, 402–408. [Google Scholar] [CrossRef] [PubMed]
- Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. 2002, 3. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Grabherr, M.G.; Haas, B.J.; Yassour, M.; Levin, J.Z.; Thompson, D.A.; Amit, I.; Adiconis, X.; Fan, L.; Raychowdhury, R.; Zeng, Q.D.; et al. Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat. Biotechnol. 2011, 29, 644. [Google Scholar] [CrossRef] [PubMed]
- Li, H.; Durbin, R. Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 2010, 26, 589–595. [Google Scholar] [CrossRef] [PubMed]
- McKenna, A.; Hanna, M.; Banks, E.; Sivachenko, A.; Cibulskis, K.; Kernytsky, A.; Garimella, K.; Altshuler, D.; Gabriel, S.; Daly, M.; et al. The genome analysis toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 2010, 20, 1297–1303. [Google Scholar] [CrossRef] [PubMed]
- Yugandhar, K.; Gromiha, M.M. Protein-protein binding affinity prediction from amino acid sequence. Bioinformatics 2014, 30, 3583–3589. [Google Scholar] [CrossRef]
- Sloan, D.B. Using plants to elucidate the mechanisms of cytonuclear co-evolution. New Phytol. 2015, 205, 1040–1046. [Google Scholar] [CrossRef]
- Ge, X.H.; Ding, L.; Li, Z.Y. Nucleolar dominance and different genome behaviors in hybrids and allopolyploids. Plant Cell Rep. 2013, 32, 1661–1673. [Google Scholar] [CrossRef]
- Sehrish, T.; Symonds, V.V.; Soltis, D.E.; Soltis, P.S.; Tate, J.A. Cytonuclear coordination is not immediate upon allopolyploid formation in Tragopogon miscellus (Asteraceae) allopolyploids. Plos ONE 2015, 10, e0144339. [Google Scholar] [CrossRef]
- Adams, K.L.; Cronn, R.; Percifield, R.; Wendel, J.F. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing. Proc. Natl. Acad. Sci. USA 2003, 100, 4649–4654. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.T.; Zhang, H.K.; Li, Y.L.; Zhang, Z.B.; Li, L.F.; Liu, B. Transcriptome asymmetry in synthetic and natural allotetraploid wheats, revealed by RNA-sequencing. New Phytol. 2016, 209, 1264–1277. [Google Scholar] [CrossRef] [PubMed]
- Barker, M.S.; Arrigo, N.; Baniaga, A.E.; Li, Z.; Levin, D.A. On the relative abundance of autopolyploids and allopolyploids. New Phytol. 2016, 210, 391–398. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.J. Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant. Sci. 2010, 15, 57–71. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Homoeolog | SNP:393 | SNP:430 | |
---|---|---|---|
HHCC-1 | H Subtotal | 687 | 687 |
C Subtotal | 959 | 805 | |
Total | 1646 | 1445 | |
HHCC-2 | H Subtotal | 458 | 359 |
C Subtotal | 603 | 439 | |
Total | 1061 | 794 | |
HHCC-3 | H Subtotal | 440 | 369 |
C Subtotal | 660 | 558 | |
Total | 1100 | 927 |
rbcL | rbcS | Kd (Dissociation Constant) | ΔG (Binding Free Energy) |
---|---|---|---|
rbcL HHCC | rbcS HHCC-H | 1.51·10-07 M | −9.30 kcal/mol |
rbcS HHCC-C | 6.87·10−08 M | −9.77 kcal/mol | |
rbcL HH | rbcS HH | 9.30·10−09 M | −10.95 kcal/mol |
rbcL CC | rbcS CC | 8.19·10−09 M | −11.03 kcal/mol |
HH | HHCC | CC | MPH (%) | |
---|---|---|---|---|
RuBisCO content (ng/g FW) | 1.41 ± 0.03 | 1.70 ± 0.03 | 1.77 ± 0.02 | 6.90% |
RuBisCO activity (μmol/min/g FW) | 7.24 ± 0.17 | 6.86 ± 0.10 | 4.76 ± 0.14 | 14.32% |
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Zhai, Y.; Yu, X.; Zhu, Z.; Wang, P.; Meng, Y.; Zhao, Q.; Li, J.; Chen, J. Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid. Genes 2019, 10, 869. https://doi.org/10.3390/genes10110869
Zhai Y, Yu X, Zhu Z, Wang P, Meng Y, Zhao Q, Li J, Chen J. Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid. Genes. 2019; 10(11):869. https://doi.org/10.3390/genes10110869
Chicago/Turabian StyleZhai, Yufei, Xiaqing Yu, Zaobing Zhu, Panqiao Wang, Ya Meng, Qinzheng Zhao, Ji Li, and Jinfeng Chen. 2019. "Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid" Genes 10, no. 11: 869. https://doi.org/10.3390/genes10110869
APA StyleZhai, Y., Yu, X., Zhu, Z., Wang, P., Meng, Y., Zhao, Q., Li, J., & Chen, J. (2019). Nuclear–Cytoplasmic Coevolution Analysis of RuBisCO in Synthesized Cucumis Allopolyploid. Genes, 10(11), 869. https://doi.org/10.3390/genes10110869