A Comparative Analysis of Major Cell Wall Components and Associated Gene Expression in Autotetraploid and Its Donor Diploid Rice (Oryza sativa L.) under Blast and Salt Stress Conditions
Abstract
:1. Introduction
2. Results
2.1. Alteration of Morphology and Polymer Content in Autotetraploid and Its Donor, Diploid Rice
2.2. Differential Expression Analysis of Genes Associated with Significant Cell Wall Components between Autotetraploid and Its Donor Diploid Rice
2.3. Phenotypic and Polymer Content Variation Occurred in Autotetraploid and Its Donor Diploid Rice under M. oryzae and Salt Stress Conditions
2.4. Expression of Genes Associated with Significant Cell Wall Components in Autotetraploid and Its Donor Diploid Rice under M. oryzae and Salt Stress Conditions
2.5. Correlation Analysis of Cell Wall Main Component Content and Expression Levels of Related Genes
3. Discussion
4. Materials and Methods
4.1. Plant Material and Stress Treatments
4.2. Determination of Agronomic Traits
4.3. Determination of Lignin, Cellulose, Hemicellulose, and Pectin Content
4.4. Transmission Electron Microscopy Observations
4.5. RNA Extraction and Sequencing Analysis
4.6. Statistical Analysis
4.7. qRT-PCR Validation
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Bomblies, K.; Madlung, A. Polyploidy in the Arabidopsis genus. Chromosome Res. 2014, 22, 117–134. [Google Scholar] [CrossRef] [PubMed]
- Soltis, P.S.; Soltis, D.E. Ancient WGD events as drivers of key innovations in angiosperms. Curr. Opin. Plant Biol. 2016, 30, 159–165. [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]
- Segraves, K.A. The effects of genome duplications in a community context. N. Phytol. 2017, 215, 57–69. [Google Scholar] [CrossRef] [PubMed]
- Lavania, U.C.; Srivastava, S.; Lavania, S.; Basu, S.; Misra, N.K.; Mukai, Y. Autopolyploidy differentially influences body size in plants, but facilitates enhanced accumulation of secondary metabolites, causing increased cytosine methylation. Plant J. 2012, 71, 539–549. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Liu, H.; Gao, A.; Yang, X.; Liu, W.; Li, X.; Li, L. Intergenomic Rearrangements after Polyploidization of Kengyilia thoroldiana (Poaceae: Triticeae) Affected by Environmental Factors. PLoS ONE 2012, 7, e31033. [Google Scholar] [CrossRef] [PubMed]
- Emery, M.; Willis, M.M.S.; Hao, Y.; Barry, K.; Oakgrove, K.; Peng, Y.; Schmutz, J.; Lyons, E.; Pires, J.C.; Edger, P.P.; et al. Preferential retention of genes from one parental genome after polyploidy illustrates the nature and scope of the genomic conflicts induced by hybridization. PLoS Genet. 2018, 14, e1007267. [Google Scholar] [CrossRef]
- Zhou, C.; Liu, X.; Li, X.; Zhou, H.; Wang, S.; Yuan, Z.; Zhang, Y.; Li, S.; You, A.; Zhou, L.; et al. A Genome Doubling Event Reshapes Rice Morphology and Products by Modulating Chromatin Signatures and Gene Expression Profiling. Rice 2021, 14, 72. [Google Scholar] [CrossRef]
- Tossi, V.E.; Martínez Tosar, L.J.; Laino, L.E.; Iannicelli, J.; Regalado, J.J.; Escandón, A.S.; Baroli, I.; Causin, H.F.; Pitta-Álvarez, S.I. Impact of polyploidy on plant tolerance to abiotic and biotic stresses. Front. Plant Sci. 2022, 13, 869423. [Google Scholar] [CrossRef]
- Schoenfelder, K.P.; Fox, D.T. The expanding implications of polyploidy. J. Cell Biol. 2015, 209, 485–491. [Google Scholar] [CrossRef]
- De Smet, R.; Sabaghian, E.; Li, Z.; Saeys, Y.; Van de Peer, Y. Coordinated Functional Divergence of Genes after Genome Duplication in Arabidopsis thaliana. Plant Cell 2017, 29, 2786–2800. [Google Scholar] [CrossRef]
- Singla, J.; Krattinger, S.G. Biotic Stress Resistance Genes in Wheat. In Reference Module in Food Science; Elsevier: Amsterdam, The Netherlands, 2016. [Google Scholar] [CrossRef]
- Gong, Z.; Xiong, L.; Shi, H.; Yang, S.; Herrera-Estrella, L.R.; Xu, G.; Chao, D.-Y.; Li, J.; Wang, P.-Y.; Qin, F.; et al. Plant abiotic stress response and nutrient use efficiency. Sci. China Life Sci. 2020, 63, 635–674. [Google Scholar] [CrossRef]
- Wang, L.; Cao, S.; Wang, P.; Lu, K.; Song, Q.; Zhao, F.-J.; Chen, Z.J. DNA hypomethylation in tetraploid rice potentiates stress-responsive gene expression for salt tolerance. Proc. Natl. Acad. Sci. USA 2021, 118, e2023981118. [Google Scholar] [CrossRef]
- Mehlferber, E.C.; Song, M.J.; Pelaez, J.N.; Jaenisch, J.; Coate, J.E.; Koskella, B.; Rothfels, C.J. Polyploidy and microbiome associations mediate similar responses to pathogens in Arabidopsis. Curr. Biol. 2022, 32, 2719–2729.e2715. [Google Scholar] [CrossRef]
- Caffall, K.H.; Mohnen, D. The structure, function, and biosynthesis of plant cell wall pectic polysaccharides. Carbohydr. Res. 2009, 344, 1879–1900. [Google Scholar] [CrossRef] [PubMed]
- Houston, K.; Tucker, M.R.; Chowdhury, J.; Shirley, N.; Little, A. The Plant Cell Wall: A Complex and Dynamic Structure As Revealed by the Responses of Genes under Stress Conditions. Front. Plant Sci. 2016, 7, 984. [Google Scholar] [CrossRef] [PubMed]
- Voxeur, A.; Höfte, H. Cell wall integrity signaling in plants: “To grow or not to grow that’s the question”. Glycobiology 2016, 26, 950–960. [Google Scholar] [CrossRef] [PubMed]
- Coutinho, F.S.; Rodrigues, J.M.; Lima, L.L.; Mesquita, R.O.; Carpinetti, P.A.; Machado, J.P.B.; Vital, C.E.; Vidigal, P.M.; Ramos, M.E.S.; Maximiano, M.R.; et al. Remodeling of the cell wall as a drought-tolerance mechanism of a soybean genotype revealed by global gene expression analysis. Abiotech 2021, 2, 14–31. [Google Scholar] [CrossRef] [PubMed]
- Zhu, Q.; Gao, P.; Liu, S.; Zhu, Z.; Amanullah, S.; Davis, A.R.; Luan, F. Comparative transcriptome analysis of two contrasting watermelon genotypes during fruit development and ripening. BMC Genom. 2017, 18, 3. [Google Scholar] [CrossRef]
- Zhao, Q.; Dixon, R.A. Transcriptional networks for lignin biosynthesis: More complex than we thought? Trends Plant Sci. 2011, 16, 227–233. [Google Scholar] [CrossRef] [PubMed]
- Liu, Q.; Luo, L.; Zheng, L. Lignins: Biosynthesis and Biological Functions in Plants. Int. J. Mol. Sci. 2018, 19, 335. [Google Scholar] [CrossRef] [PubMed]
- Moura, J.C.M.S.; Bonine, C.A.V.; de Oliveira Fernandes Viana, J.; Dornelas, M.C.; Mazzafera, P. Abiotic and Biotic Stresses and Changes in the Lignin Content and Composition in Plants. J. Integr. Plant Biol. 2010, 52, 360–376. [Google Scholar] [CrossRef] [PubMed]
- Liu, H.; Guo, Z.; Gu, F.; Ke, S.; Sun, D.; Dong, S.; Liu, W.; Huang, M.; Xiao, W.; Yang, G.; et al. 4-Coumarate-CoA Ligase-Like Gene OsAAE3 Negatively Mediates the Rice Blast Resistance, Floret Development and Lignin Biosynthesis. Front. Plant Sci. 2017, 7, 2041. [Google Scholar] [CrossRef] [PubMed]
- Chen, K.; Song, M.; Guo, Y.; Liu, L.; Xue, H.; Dai, H.; Zhang, Z. MdMYB46 could enhance salt and osmotic stress tolerance in apple by directly activating stress-responsive signals. Plant Biotechnol. J. 2019, 17, 2341–2355. [Google Scholar] [CrossRef]
- Mohnen, D. Pectin structure and biosynthesis. Curr. Opin. Plant Biol. 2008, 11, 266–277. [Google Scholar] [CrossRef] [PubMed]
- Yan, J.; He, H.; Fang, L.; Zhang, A. Pectin methylesterase31 positively regulates salt stress tolerance in Arabidopsis. Biochem. Biophys. Res. Commun. 2018, 496, 497–501. [Google Scholar] [CrossRef] [PubMed]
- Ohara, T.; Takeuchi, H.; Sato, J.; Nakamura, A.; Ichikawa, H.; Yokoyama, R.; Nishitani, K.; Minami, E.; Satoh, S.; Iwai, H. Structural Alteration of Rice Pectin Affects Cell Wall Mechanical Strength and Pathogenicity of the Rice Blast Fungus Under Weak Light Conditions. Plant Cell Physiol. 2021, 62, 641–649. [Google Scholar] [CrossRef]
- Lin, S.; Miao, Y.; Huang, H.; Zhang, Y.; Huang, L.; Cao, J. Arabinogalactan Proteins: Focus on the Role in Cellulose Synthesis and Deposition during Plant Cell Wall Biogenesis. Int. J. Mol. Sci. 2022, 23, 6578. [Google Scholar] [CrossRef]
- Kumar, M.; Turner, S. Plant cellulose synthesis: CESA proteins crossing kingdoms. Phytochemistry 2015, 112, 91–99. [Google Scholar] [CrossRef]
- McFarlane, H.E.; Döring, A.; Persson, S. The Cell Biology of Cellulose Synthesis. Annu. Rev. Plant Biol. 2014, 65, 69–94. [Google Scholar] [CrossRef]
- Pedersen, G.B.; Blaschek, L.; Frandsen, K.E.H.; Noack, L.C.; Persson, S. Cellulose synthesis in land plants. Mol. Plant 2023, 16, 206–231. [Google Scholar] [CrossRef]
- Zhao, H.; Li, Z.; Wang, Y.; Wang, J.; Xiao, M.; Liu, H.; Quan, R.; Zhang, H.; Huang, R.; Zhu, L.; et al. Cellulose synthase-like protein OsCSLD4 plays an important role in the response of rice to salt stress by mediating abscisic acid biosynthesis to regulate osmotic stress tolerance. Plant Biotechnol. J. 2022, 20, 468–484. [Google Scholar] [CrossRef] [PubMed]
- Kesten, C.; Menna, A.; Sánchez-Rodríguez, C. Regulation of cellulose synthesis in response to stress. Curr. Opin. Plant Biol. 2017, 40, 106–113. [Google Scholar] [CrossRef] [PubMed]
- Pauly, M.; Gille, S.; Liu, L.; Mansoori, N.; de Souza, A.; Schultink, A.; Xiong, G. Hemicellulose biosynthesis. Planta 2013, 238, 627–642. [Google Scholar] [CrossRef] [PubMed]
- Scheller, H.V.; Ulvskov, P. Hemicelluloses. Annu. Rev. Plant Biol. 2010, 61, 263–289. [Google Scholar] [CrossRef]
- Le Gall, H.; Philippe, F.; Domon, J.-M.; Gillet, F.; Pelloux, J.; Rayon, C. Cell Wall Metabolism in Response to Abiotic Stress. Plants 2015, 4, 112–166. [Google Scholar] [CrossRef] [PubMed]
- Yang, C.; Liu, R.; Pang, J.; Ren, B.; Zhou, H.; Wang, G.; Wang, E.; Liu, J. Poaceae-specific cell wall-derived oligosaccharides activate plant immunity via OsCERK1 during Magnaporthe oryzae infection in rice. Nat. Commun. 2021, 12, 2178. [Google Scholar] [CrossRef] [PubMed]
- Sattler, M.C.; Carvalho, C.R.; Clarindo, W.R. The polyploidy and its key role in plant breeding. Planta 2015, 243, 281–296. [Google Scholar] [CrossRef]
- Nassar, N.M.A.; Graciano-Ribeiro, D.; Fernandes, S.D.C.; Araujo, P.C. Anatomical alterations due to polyploidy in cassava, Manihot esculenta Crantz. Genet. Mol. Res. 2008, 7, 276–283. [Google Scholar] [CrossRef]
- Wu, K.; Xu, E.; Fan, G.; Niu, S.; Zhao, Z.; Deng, M.; Dong, Y. Transcriptome-Wide Profiling and Expression Analysis of Diploid and Autotetraploid Paulownia tomentosa × Paulownia fortunei under Drought Stress. PLoS ONE 2014, 9, e113313. [Google Scholar] [CrossRef]
- Serapiglia, M.J.; Gouker, F.E.; Hart, J.F.; Unda, F.; Mansfield, S.D.; Stipanovic, A.J.; Smart, L.B. Ploidy Level Affects Important Biomass Traits of Novel Shrub Willow (Salix) Hybrids. BioEnergy Res. 2014, 8, 259–269. [Google Scholar] [CrossRef]
- Hernández-Blanco, C.; Feng, D.X.; Hu, J.; Sánchez-Vallet, A.; Deslandes, L.; Llorente, F.; Berrocal-Lobo, M.; Keller, H.; Barlet, X.; Sánchez-Rodríguez, C.; et al. Impairment of Cellulose Synthases Required forArabidopsisSecondary Cell Wall Formation Enhances Disease Resistance. Plant Cell 2007, 19, 890–903. [Google Scholar] [CrossRef]
- Malinovsky, F.G.; Fangel, J.U.; Willats, W.G.T. The role of the cell wall in plant immunity. Front. Plant Sci. 2014, 5, 178. [Google Scholar] [CrossRef]
- Hamann, T. The Plant Cell Wall Integrity Maintenance Mechanism—Concepts for Organization and Mode of Action. Plant Cell Physiol. 2014, 56, 215–223. [Google Scholar] [CrossRef]
- Li, W.; Wang, K.; Chern, M.; Liu, Y.; Zhu, Z.; Liu, J.; Zhu, X.; Yin, J.; Ran, L.; Xiong, J.; et al. Sclerenchyma cell thickening through enhanced lignification induced by OsMYB30 prevents fungal penetration of rice leaves. N. Phytol. 2020, 226, 1850–1863. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Zhang, W.; Long, S.; Zhao, C. Maintenance of Cell Wall Integrity under High Salinity. Int. J. Mol. Sci. 2021, 22, 3260. [Google Scholar] [CrossRef] [PubMed]
- Coculo, D.; Del Corpo, D.; Martínez, M.O.; Vera, P.; Piro, G.; De Caroli, M.; Lionetti, V. Arabidopsis subtilases promote defense-related pectin methylesterase activity and robust immune responses to botrytis infection. Plant Physiol. Biochem. 2023, 201, 107865. [Google Scholar] [CrossRef] [PubMed]
- Dabravolski, S.A.; Isayenkov, S.V. The regulation of plant cell wall organisation under salt stress. Front. Plant Sci. 2023, 14, 4609. [Google Scholar] [CrossRef] [PubMed]
- Dorokhov, Y.L.; Sheshukova, E.V.; Komarova, T.V. Methanol in Plant Life. Front. Plant Sci. 2018, 9, 1623. [Google Scholar] [CrossRef]
- Tanaka, K.; Murata, K.; Yamazaki, M.; Onosato, K.; Miyao, A.; Hirochika, H. Three Distinct Rice Cellulose Synthase Catalytic Subunit Genes Required for Cellulose Synthesis in the Secondary Wall. Plant Physiol. 2003, 133, 73–83. [Google Scholar] [CrossRef]
- Wang, D.; Yuan, S.; Yin, L.; Zhao, J.; Guo, B.; Lan, J.; Li, X. A missense mutation in the transmembrane domain of CESA9 affects cell wall biosynthesis and plant growth in rice. Plant Sci. 2012, 196, 117–124. [Google Scholar] [CrossRef]
- Li, Y.; Wang, R.; Pei, Y.; Yu, W.; Wu, W.; Li, D.; Hu, Z. Phylogeny and functional characterization of the cinnamyl alcohol dehydrogenase gene family in Phryma leptostachya. Int. J. Biol. Macromol. 2022, 217, 407–416. [Google Scholar] [CrossRef]
- Huang, M.T.; Lu, Y.C.; Zhang, S.; Luo, F.; Yang, H. Rice (Oryza sativa) Laccases Involved in Modification and Detoxification of Herbicides Atrazine and Isoproturon Residues in Plants. J. Agric. Food Chem. 2016, 64, 6397–6406. [Google Scholar] [CrossRef]
- Wang, L.; Yuan, J.; Ma, Y.; Jiao, W.; Ye, W.; Yang, D.-L.; Yi, C.; Chen, Z.J. Rice Interploidy Crosses Disrupt Epigenetic Regulation, Gene Expression, and Seed Development. Mol. Plant 2018, 11, 300–314. [Google Scholar] [CrossRef]
- Qu, S.; Liu, G.; Zhou, B.; Bellizzi, M.; Zeng, L.; Dai, L.; Han, B.; Wang, G.-L. The Broad-Spectrum Blast Resistance Gene Pi9 Encodes a Nucleotide-Binding Site–Leucine-Rich Repeat Protein and Is a Member of a Multigene Family in Rice. Genetics 2006, 172, 1901–1914. [Google Scholar] [CrossRef]
- Kim, D.; Langmead, B.; Salzberg, S.L. HISAT: A fast spliced aligner with low memory requirements. Nat. Methods 2015, 12, 357–360. [Google Scholar] [CrossRef]
- Tang, Q.-Y.; Zhang, C.-X. Data Processing System (DPS) software with experimental design, statistical analysis and data mining developed for use in entomological research. Insect Sci. 2013, 20, 254–260. [Google Scholar] [CrossRef]
- Chen, C.; Chen, H.; Zhang, Y.; Thomas, H.R.; Frank, M.H.; He, Y.; Xia, R. TBtools: An Integrative Toolkit Developed for Interactive Analyses of Big Biological Data. Mol. Plant 2020, 13, 1194–1202. [Google Scholar] [CrossRef]
- Wang, N.; Fan, X.; Lin, Y.; Li, Z.; Wang, Y.; Zhou, Y.; Meng, W.; Peng, Z.; Zhang, C.; Ma, J. Alkaline Stress Induces Different Physiological, Hormonal and Gene Expression Responses in Diploid and Autotetraploid Rice. Int. J. Mol. Sci. 2022, 23, 5561. [Google Scholar] [CrossRef]
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Leng, Z.; Liu, K.; Wang, C.; Qi, F.; Zhang, C.; Li, D.; Wang, N.; Ma, J. A Comparative Analysis of Major Cell Wall Components and Associated Gene Expression in Autotetraploid and Its Donor Diploid Rice (Oryza sativa L.) under Blast and Salt Stress Conditions. Plants 2023, 12, 3976. https://doi.org/10.3390/plants12233976
Leng Z, Liu K, Wang C, Qi F, Zhang C, Li D, Wang N, Ma J. A Comparative Analysis of Major Cell Wall Components and Associated Gene Expression in Autotetraploid and Its Donor Diploid Rice (Oryza sativa L.) under Blast and Salt Stress Conditions. Plants. 2023; 12(23):3976. https://doi.org/10.3390/plants12233976
Chicago/Turabian StyleLeng, Zitian, Keyan Liu, Chenxi Wang, Fan Qi, Chunying Zhang, Dayong Li, Ningning Wang, and Jian Ma. 2023. "A Comparative Analysis of Major Cell Wall Components and Associated Gene Expression in Autotetraploid and Its Donor Diploid Rice (Oryza sativa L.) under Blast and Salt Stress Conditions" Plants 12, no. 23: 3976. https://doi.org/10.3390/plants12233976