Discover the SciOpen Platform and Achieve Your Research Goals with Ease.
Search articles, authors, keywords, DOl and etc.
Cotton is a major crop that provides the most important renewable textile fibers in the world. Studies of the taxonomy and evolution of cotton species have received wide attentions, not only due to cotton’s economic value but also due to the fact that Gossypium is an ideal model system to study the origin, evolution, and cultivation of polyploid species. Previous studies suggested the involvement of mitochondrial genome editing sites and copy number as well as mitochondrial functions in cotton fiber elongation. Whereas, with only a few mitogenomes assembled in the cotton genus Gossypium, our knowledge about their roles in cotton evolution and speciation is still scarce. To close this gap, here we assembled 20 mitogenomes from 15 cotton species spanning all the cotton clades (A–G, K, and AD genomes) and 5 cotton relatives using short and long sequencing reads. Systematic analyses uncovered a high level of mitochondrial gene sequence conservation, abundant sequence repeats and many insertions of foreign sequences, as well as extensive structural variations in cotton mitogenomes. The sequence repeats and foreign sequences caused significant mitogenome size inflation in Gossypium and its close relative Kokia in general, while there is no significant difference between the lint and fuzz cotton mitogenomes in terms of gene content, RNA editing, and gene expression level. Interestingly, we further revealed the specific presence and expression of two novel mitochondrial open reading frames (ORFs) in lint-fiber cotton species. Finally, these structural features and novel ORFs help us gain valuable insights into the history of cotton evolution and polyploidization and the origin of species producing long lint fibers from a mitogenomic perspective.
J.F. Wendel, R.C. Cronn, Polyploidy and the evolutionary history of cotton, Adv. Agron. 78 (2003) 139–186.
J.F. Wendel, New World tetraploid cottons contain Old World cytoplasm, Proc. Natl. Acad. Sci. U. S. A. 86 (1989) 4132–4136.
W.L. Applequist, R. Cronn, J.F. Wendel, Comparative development of fiber in wild and cultivated cotton, Evol. Dev. 3 (2001) 3–17.
Y. Pang, H. Wang, W.Q. Song, Y.X. Zhu, The cotton ATP synthase δ1 subunit is required to maintain a higher ATP/ADP ratio that facilitates rapid fibre cell elongation, Plant Biol. 12 (2010) 903–909.
P. He, G. Xiao, H. Liu, L. Zhang, L.I. Zhao, M. Tang, S. Huang, Y. An, J. Yu, Two pivotal RNA editing sites in the mitochondrial atp1mRNA are required for ATP synthase to produce sufficient ATP for cotton fiber cell elongation, New Phytol. 218 (2018) 167–182.
J.P. Mower, Variation in protein gene and intron content among land plant mitogenomes, Mitochondrion 53 (2020) 203–213.
G.N. Thyssen, X. Song, M. Naoumkina, H.J. Kim, D.D. Fang, Independent replication of mitochondrial genes supports the transcriptional program in developing fiber cells of cotton, (Gossypium hirsutum) L., Gene 544 (2014) 41–48.
G.N. Thyssen, D.D. Fang, L. Zeng, X. Song, C.D. Delhom, T.L. Condon, P. Li, H.J. Kim, The immature fiber mutant phenotype of cotton (Gossypium hirsutum) is linked to a 22-bp frame-shift deletion in a mitochondria targeted pentatricopeptide repeat gene, G3-Genes Genomes Genet. 6 (2016) 1627–1633.
D. Zhang, C. Chen, H. Wang, E. Niu, P. Zhao, S. Fang, G. Zhu, X. Shang, W. Guo, Cotton fiber development requires the pentatricopeptide repeat protein ghim for splicing of mitochondrial nad7 mRNA, Genetics 217 (2021) 1–17.
C.J. Dong, A.M. Wu, S.J. Du, K. Tang, Y. Wang, J.Y. Liu, GhMCS1, the cotton orthologue of human GRIM-19, is a subunit of mitochondrial complex I and associated with cotton fibre growth, PLoS ONE 11 (2016) e0162928.
J. Yu, S. Jung, C.H. Cheng, S.P. Ficklin, T. Lee, P. Zheng, D. Jones, R.G. Percy, D. Main, CottonGen: a genomics, genetics and breeding database for cotton research, Nucleic Acids Res. 42 (2014) D1229–1236.
Y. Wu, F. Liu, D.G. Yang, W. Li, X.J. Zhou, X.Y. Pei, Y.G. Liu, K.L. He, W.S. Zhang, Z. Y. Ren, K.H. Zhou, X.F. Ma, Z.H. Li, Comparative chloroplast genomics of Gossypium species: insights into repeat sequence variations and phylogeny, Front. Plant Sci. 9 (2018) 376.
B. Lei, S. Li, G. Liu, Z. Chen, A. Su, P. Li, Z. Li, J. Hua, Evolution of mitochondrial gene content: loss of genes, tRNAs and introns between Gossypium harknessii and other plants, Plant Syst. Evol. 299 (2013) 1889–1897.
G. Liu, D. Cao, S. Li, A. Su, J. Geng, C.E. Grover, S. Hu, J. Hua, The complete mitochondrial genome of Gossypium hirsutum and evolutionary analysis of higher plant mitochondrial genomes, PLoS ONE 8 (2013) e69476.
M. Tang, Z. Chen, C.E. Grover, Y. Wang, S. Li, G. Liu, Z. Ma, J.F. Wendel, J. Hua, Rapid evolutionary divergence of Gossypium barbadense and G. hirsutum mitochondrial genomes, BMC Genomics 16 (2015) 770.
Z. Chen, N. Zhao, S. Li, C.E. Grover, H. Nie, J.F. Wendel, J. Hua, Plant mitochondrial genome evolution and cytoplasmic male sterility, Crit. Rev. Plant Sci. 36 (2017) 55–69.
F. Budar, G. Pelletier, Male sterility in plants: occurrence, determinism, significance and use, C. R. Acad. Sci. Ⅲ 324 (2001) 543–550.
G. Huang, Z. Wu, R.G. Percy, M. Bai, Y. Li, J.E. Frelichowski, J. Hu, K. Wang, J.Z. Yu, Y. Zhu, Genome sequence of Gossypium herbaceum and genome updates of Gossypium arboreum and Gossypium hirsutum provide insights into cotton A-genome evolution, Nat. Genet. 52 (2020) 516–524.
M. Kolmogorov, J. Yuan, Y.U. Lin, P.A. Pevzner, Assembly of long, error-prone reads using repeat graphs, Nat. Biotechnol. 37 (2019) 540–546.
C. Camacho, G. Coulouris, V. Avagyan, N. Ma, J. Papadopoulos, K. Bealer, T.L. Madden, BLAST+: architecture and applications, BMC Bioinformatics 10 (2009) 421
Y. Feng, X. Xiang, D. Akhter, R. Pan, Z. Fu, X. Jin, Mitochondrial phylogenomics of fagales provides insights into plant mitogenome mosaic evolution, Front. Plant Sci. 12 (2021) 762195.
A.M. Bolger, M. Lohse, B. Usadel, Trimmomatic: a flexible trimmer for Illumina sequence data, Bioinformatics 30 (2014) 2114–2120.
A. Bankevich, S. Nurk, D. Antipov, A.A. Gurevich, M. Dvorkin, A.S. Kulikov, V.M. Lesin, S.I. Nikolenko, S. Pham, A.D. Prjibelski, A.V. Pyshkin, A.V. Sirotkin, N. Vyahhi, G. Tesler, M.A. Alekseyev, P.A. Pevzner, SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing, J. Comput. Biol. 19 (2012) 455–477.
M. Krzywinski, J. Schein, I. Birol, J. Connors, R. Gascoyne, D. Horsman, S.J. Jones, M.A. Marra, Circos: an information aesthetic for comparative genomics, Genome Res. 19 (2009) 1639–1645.
K. Katoh, D.M. Standley, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol. Biol. Evol. 30 (2013) 772–780.
L.T. Nguyen, H.A. Schmidt, A. von Haeseler, B.Q. Minh, IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies, Mol. Biol. Evol. 32 (2015) 268–274.
Y. Hu, J. Chen, L. Fang, Z. Zhang, W. Ma, Y. Niu, L. Ju, J. Deng, T. Zhao, J. Lian, K. Baruch, D. Fang, X. Liu, Y.L. Ruan, M.U. Rahman, J. Han, K. Wang, Q. Wang, H. Wu, G. Mei, Y. Zang, Z. Han, C. Xu, W. Shen, D. Yang, Z. Si, F. Dai, L. Zou, F. Huang, Y. Bai, Y. Zhang, A. Brodt, H. Ben-Hamo, X. Zhu, B. Zhou, X. Guan, S. Zhu, X. Chen, T. Zhang, Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton, Nat. Genet. 51 (2019) 739–748.
C.E. Grover, D. Yuan, M.A. Arick, E.R. Miller, G. Hu, D.G. Peterson, J.F. Wendel, J. A. Udall, The Gossypium anomalum genome as a resource for cotton improvement and evolutionary analysis of hybrid incompatibility, G3-Genes Genomes Genet. 11 (2021) jkab319.
Z. Yang, X. Ge, W. Li, Y. Jin, L. Liu, W. Hu, F. Liu, Y. Chen, S. Peng, F. Li, Cotton D genome assemblies built with long-read data unveil mechanisms of centromere evolution and stress tolerance divergence, BMC Biol. 19 (2021) 115.
M. Wang, J. Li, P. Wang, F. Liu, Z. Liu, G. Zhao, Z. Xu, L. Pei, C.E. Grover, J.F. Wendel, K. Wang, X. Zhang, Comparative genome analyses highlight transposon-mediated genome expansion and the evolutionary architecture of 3D genomic folding in cotton, Mol. Biol. Evol. 38 (2021) 3621–3636.
C.E. Grover, M. Pan, D. Yuan, M.A. Arick, G. Hu, L. Brase, D.M. Stelly, Z. Lu, R.J. Schmitz, D.G. Peterson, J.F. Wendel, J.A. Udall, The Gossypium longicalyx genome as a resource for cotton breeding and evolution, G3-Genes Genomes Genet. 10 (2020) 1457–1467.
J.A. Udall, E. Long, T. Ramaraj, J.L. Conover, D. Yuan, C.E. Grover, L. Gong, M.A. Arick, R.E. Masonbrink, D.G. Peterson, J.F. Wendel, The genome sequence of Gossypioides kirkii illustrates a descending dysploidy in plants, Front. Plant Sci. 10 (2019) 1541.
S.C. Boon, L. Lim, Organelle transcriptomes in plants, Transcriptomics 2 (2013) 1000e106.
T. Zhao, X. Tao, S. Feng, L. Wang, H. Hong, W. Ma, G. Shang, S. Guo, Y. He, B. Zhou, X. Guan, LncRNAs in polyploid cotton interspecific hybrids are derived from transposon neofunctionalization, Genome Biol. 19 (2018) 195.
D. Kim, J.M. Paggi, C. Park, C. Bennett, S.L. Salzberg, Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype, Nat. Biotechnol. 37 (2019) 907–915.
S. Anders, P.T. Pyl, W. Huber, HTSeq—a Python framework to work with high-throughput sequencing data, Bioinformatics 31 (2015) 166–169.
Z. Chen, K. Feng, C.E. Grover, P. Li, F. Liu, Y. Wang, Q. Xu, M. Shang, Z. Zhou, X. Cai, X. Wang, J.F. Wendel, K. Wang, J. Hua, Chloroplast DNA structural variation, phylogeny, and age of divergence among diploid cotton species, PLoS ONE 11 (2016) e0157183.
Z. Chen, C.E. Grover, P. Li, Y. Wang, H. Nie, Y. Zhao, M. Wang, F. Liu, Z. Zhou, X. Wang, X. Cai, K. Wang, J.F. Wendel, J. Hua, Molecular evolution of the plastid genome during diversification of the cotton genus, Mol. Phylogenet. Evol. 112 (2017) 268–276.
A. Tsitrone, M. Kirkpatrick, D.A. Levin, A model for chloroplast capture, Evolution 57 (2003) 1776–1782.
T. Kazama, M. Okuno, Y. Watari, S. Yanase, C. Koizuka, Y. Tsuruta, H. Sugaya, A. Toyoda, T. Itoh, N. Tsutsumi, K. Toriyama, N. Koizuka, S. ichi Arimura,, Curing cytoplasmic male sterility via TALEN-mediated mitochondrial genome editing, Nat. Plants 5 (2019) 722–730.
S. Li, Z. Chen, N. Zhao, Y. Wang, H. Nie, J. Hua, The comparison of four mitochondrial genomes reveals cytoplasmic male sterility candidate genes in cotton, BMC Genomics 19 (2018) 775.
S. O’Conner, L. Li, Mitochondrial fostering: the mitochondrial genome may play a role in plant orphan gene evolution, Front. Plant Sci. 11 (2020) 600117.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).