Cytonuclear evolution in fully heterotrophic plants: lifestyles and gene function determine scenarios.

Heterotrophic Processes Evolution, Molecular Cell Nucleus / genetics Genes, Plant Plastids / genetics
Cytonuclear coevolution Endoparasite Gene loss Mycoheterotroph Substitution rate

Journal

BMC plant biology
ISSN: 1471-2229
Titre abrégé: BMC Plant Biol
Pays: England
ID NLM: 100967807

Informations de publication

Date de publication:
21 Oct 2024
Historique:
received: 08 08 2024
accepted: 14 10 2024
medline: 21 10 2024
pubmed: 21 10 2024
entrez: 20 10 2024
Statut: epublish

Résumé

Evidence shows that full mycoheterotrophs and holoparasites often have reduced plastid genomes with rampant gene loss, elevated substitution rates, and deeply altered to conventional evolution in mitochondrial genomes, but mechanisms of cytonuclear evolution is unknown. Endoparasitic Sapria himalayana and mycoheterotrophic Gastrodia and Platanthera guangdongensis represent different heterotrophic types, providing a basis to illustrate cytonuclear evolution. Here, we focused on nuclear-encoded plastid / mitochondrial (N-pt / mt) -targeting protein complexes, including caseinolytic protease (ClpP), ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo), oxidative phosphorylation system (OXPHOS), DNA recombination, replication, and repair (DNA-RRR) system, and pentatricopeptide repeat (PPR) proteins, to identify evolutionary drivers for cytonuclear interaction. The severity of gene loss of N-pt PPR and pt-RRR genes was positively associated with increased degree of heterotrophy in full mycoheterotrophs and S. himalayana, while N-mt PPR and mt-RRR genes were retained. Substitution rates of organellar and nuclear genes encoding N-pt/mt subunits in protein complexes were evaluated, cytonuclear coevolution was identified in S. himalayana, whereas disproportionate rates of evolution were observed in the OXPHOS complex in full mycoheterotrophs, only slight accelerations in substitution rates were identified in N-mt genes of full mycoheterotrophs. Nuclear compensatory evolution was identified in protein complexes encoded by plastid and N-pt genes. Selection shaping codon preferences, functional constraint, mt-RRR gene regulation, and post-transcriptional regulation of PPR genes all facilitate mito-nuclear evolution. Our study enriches our understanding of genomic coevolution scenarios in fully heterotrophic plants.

Sections du résumé

BACKGROUND BACKGROUND
Evidence shows that full mycoheterotrophs and holoparasites often have reduced plastid genomes with rampant gene loss, elevated substitution rates, and deeply altered to conventional evolution in mitochondrial genomes, but mechanisms of cytonuclear evolution is unknown. Endoparasitic Sapria himalayana and mycoheterotrophic Gastrodia and Platanthera guangdongensis represent different heterotrophic types, providing a basis to illustrate cytonuclear evolution. Here, we focused on nuclear-encoded plastid / mitochondrial (N-pt / mt) -targeting protein complexes, including caseinolytic protease (ClpP), ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCo), oxidative phosphorylation system (OXPHOS), DNA recombination, replication, and repair (DNA-RRR) system, and pentatricopeptide repeat (PPR) proteins, to identify evolutionary drivers for cytonuclear interaction.
RESULTS RESULTS
The severity of gene loss of N-pt PPR and pt-RRR genes was positively associated with increased degree of heterotrophy in full mycoheterotrophs and S. himalayana, while N-mt PPR and mt-RRR genes were retained. Substitution rates of organellar and nuclear genes encoding N-pt/mt subunits in protein complexes were evaluated, cytonuclear coevolution was identified in S. himalayana, whereas disproportionate rates of evolution were observed in the OXPHOS complex in full mycoheterotrophs, only slight accelerations in substitution rates were identified in N-mt genes of full mycoheterotrophs.
CONCLUSIONS CONCLUSIONS
Nuclear compensatory evolution was identified in protein complexes encoded by plastid and N-pt genes. Selection shaping codon preferences, functional constraint, mt-RRR gene regulation, and post-transcriptional regulation of PPR genes all facilitate mito-nuclear evolution. Our study enriches our understanding of genomic coevolution scenarios in fully heterotrophic plants.

Identifiants

DOI: 10.1186/s12870-024-05702-4 PMID: 39428472
pubmed: 39428472
doi: 10.1186/s12870-024-05702-4
pii: 10.1186/s12870-024-05702-4
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

989

Informations de copyright

© 2024. The Author(s).

Références

Giegé P, Sweetlove LJ, Vr Cognat, Leaver CJ. Coordination of nuclear and mitochondrial genome expression during mitochondrial biogenesis in Arabidopsis. Plant Cell. 2005;17(5):1497–512.
pubmed: 15829605 pmcid: 1091770 doi: 10.1105/tpc.104.030254
Sloan DB, Triant DA, Wu M, Taylor DR. Cytonuclear interactions and relaxed selection accelerate sequence evolution in organelle ribosomes. Mol Biol Evol. 2014;31(3):673–82.
pubmed: 24336923 doi: 10.1093/molbev/mst259
Lian Q, Li S, Kan S, Liao X, Huang S, Sloan DB, Wu Z, Zhai W. Association analysis provides insights into plant mitonuclear interactions. Mol Biol Evol. 2024;41(2):msae028.
pubmed: 38324417 pmcid: 10875325 doi: 10.1093/molbev/msae028
Schelkunov MI, Nuraliev MS, Logacheva MD. Genomic comparison of non-photosynthetic plants from the family Balanophoraceae with their photosynthetic relatives. Peer J. 2021;9: e12106.
pubmed: 34540375 pmcid: 8415285 doi: 10.7717/peerj.12106
Ceriotti LF, Gatica-Soria L, Sanchez-Puerta MV. Cytonuclear coevolution in a holoparasitic plant with highly disparate organellar genomes. Plant Mol Biol. 2022;109(6):673–88. https://doi.org/10.1007/s11103-022-01266-9 .
doi: 10.1007/s11103-022-01266-9 pubmed: 35359176
Schmitzlinneweber C, Small I. Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci. 2008;13(12):663–70.
pubmed: 19004664 doi: 10.1016/j.tplants.2008.10.001
Sugita M. An overview of pentatricopeptide repeat (PPR) proteins in the moss Physcomitrium patens and their role in organellar gene expression. Plants. 2022;11(17):2279.
pubmed: 36079663 pmcid: 9459714 doi: 10.3390/plants11172279
Bromham L, Cowman PF, Lanfear R. Parasitic plants have increased rates of molecular evolution across all three genomes. BMC Evol Biol. 2013;13(1): 126.
pubmed: 23782527 pmcid: 3694452 doi: 10.1186/1471-2148-13-126
Havird JC, Trapp P, Miller CM, Bazos I, Sloan DB. Causes and consequences of rapidly evolving mtDNA in a plant lineage. Genome Biol Evol. 2017;9(2):323–36.
pubmed: 28164243 pmcid: 5381668 doi: 10.1093/gbe/evx010
Williams AM, Friso G, van Wijk KJ, Sloan DB. Extreme variation in rates of evolution in the plastid Clp protease complex. Plant J. 2019;98(2):243–59.
pubmed: 30570818 doi: 10.1111/tpj.14208
Hill GE. Mitonuclear compensatory coevolution. Trends Genet. 2020;36(6):403–14.
pubmed: 32396834 doi: 10.1016/j.tig.2020.03.002
Biot-Pelletier D, Bettinazzi S, Gagnon-Arsenault I, Dubé AK, Bédard C, Nguyen THM, et al. Evolutionary trajectories are contingent on mitonuclear interactions. Mol Biol Evol. 2023;40(4): msad061.
pubmed: 36929911 pmcid: 10072823 doi: 10.1093/molbev/msad061
Timilsena PR, Barrett CF, Piñeyro-Nelson A, Wafula EK, Ayyampalayam S, McNeal JR, et al. Phylotranscriptomic analyses of mycoheterotrophic monocots show a continuum of convergent evolutionary changes in expressed nuclear genes from three independent nonphotosynthetic lineages. Genome Biol Evol. 2023;15(1): evac183.
pubmed: 36582124 doi: 10.1093/gbe/evac183
Kan S, Liao X, Lan L, Kong J, Wang J, Nie L, et al. Cytonuclear interactions and subgenome dominance shape the evolution of organelle-targeted genes in the Brassica triangle of U. Mol Biol Evol. 2024;41(3):msae043.
pubmed: 38391484 pmcid: 10919925 doi: 10.1093/molbev/msae043
Cai L. Rethinking convergence in plant parasitism through the lens of molecular and population genetic processes. Am J Bot. 2023;110(5): e16174.
pubmed: 37154532 doi: 10.1002/ajb2.16174
Merckx VSFT, Gomes SIF, Wang D, Verbeek C, Jacquemyn H, Zahn FE, et al. Mycoheterotrophy in the wood-wide web. Nat Plants. 2024;10(5):710–8.
pubmed: 38641664 doi: 10.1038/s41477-024-01677-0
Roquet C, Coissac É, Cruaud C, Boleda M, Boyer F, Alberti A, et al. Understanding the evolution of holoparasitic plants: the complete plastid genome of the holoparasite Cytinus hypocistis (Cytinaceae). Ann Bot. 2016;118(5):885–96.
pubmed: 27443299 pmcid: 5055816 doi: 10.1093/aob/mcw135
Wen Y, Qin Y, Shao B, Li J, Ma C, Liu Y, et al. The extremely reduced, diverged and reconfigured plastomes of the largest mycoheterotrophic orchid lineage. BMC Plant Biol. 2022;22(1):448. https://doi.org/10.1186/s12870-022-03836-x .
doi: 10.1186/s12870-022-03836-x pubmed: 36123622 pmcid: 9487142
Graham SW, Lam VKY, Merckx VSFT. Plastomes on the edge: the evolutionary breakdown of mycoheterotroph plastid genomes. New Phytol. 2017;214(1):48–55.
pubmed: 28067952 doi: 10.1111/nph.14398
Barrett CF, Sinn BT, Kennedy AH. Unprecedented parallel photosynthetic losses in a heterotrophic Orchid genus. Mol Biol Evol. 2019;36(9):1884–901.
pubmed: 31058965 pmcid: 6736286 doi: 10.1093/molbev/msz111
Sanchez-Puerta MV, García LE, Wohlfeiler J, Ceriotti LF. Unparalleled replacement of native mitochondrial genes by foreign homologs in a holoparasitic plant. New Phytol. 2016;214(1):376–87.
pubmed: 27905116 doi: 10.1111/nph.14361
Zervas A, Petersen G, Seberg O. Mitochondrial genome evolution in parasitic plants. BMC Evol Biol. 2019;19(1):87.
pubmed: 30961535 pmcid: 6454704 doi: 10.1186/s12862-019-1401-8
Sinn BT, Barrett CF. Ancient mitochondrial gene transfer between fungi and the orchids. Mol Biol Evol. 2020;37(1):44–57.
pubmed: 31504747 doi: 10.1093/molbev/msz198
Guo X, Hu X, Li J, Shao B, Wang Y, Wang L, et al. The Sapria himalayana genome provides new insights into the lifestyle of endoparasitic plants. BMC Biol. 2023;21(1):134. https://doi.org/10.1186/s12915-023-01620-3 .
doi: 10.1186/s12915-023-01620-3 pubmed: 37280593 pmcid: 10246380
Kim Y-K, Jo S, Cheon S-H, Hong J-R, Kim K-J. Ancient horizontal gene transfers from plastome to mitogenome of a nonphotosynthetic Orchid, Gastrodia pubilabiata (Epidendroideae, Orchidaceae). Int J Mol Sci. 2023;24(14):11448.
pubmed: 37511216 pmcid: 10380568 doi: 10.3390/ijms241411448
Skippington E, Barkman TJ, Rice DW, Palmer JD. Miniaturized mitogenome of the parasitic plant Viscum scurruloideum is extremely divergent and dynamic and has lost all nad genes. Proc Natl Acad Sci USA. 2015;112(27):E3515–24.
pubmed: 26100885 pmcid: 4500244 doi: 10.1073/pnas.1504491112
Skippington E, Barkman TJ, Rice DW, Palmer JD. Comparative mitogenomics indicates respiratory competence in parasitic Viscum despite loss of complex I and extreme sequence divergence, and reveals horizontal gene transfer and remarkable variation in genome size. BMC Plant Biol. 2017;17(1):49.
pubmed: 28222679 pmcid: 5319169 doi: 10.1186/s12870-017-0992-8
Yuan Y, Jin X, Liu J, Zhao X, Zhou J, Wang X, et al. The Gastrodia elata genome provides insights into plant adaptation to heterotrophy. Nat Commun. 2018;9(1):1615.
pubmed: 29691383 pmcid: 5915607 doi: 10.1038/s41467-018-03423-5
Broz AK, Waneka G, Wu Z, Fernandes Gyorfy M, Sloan DB, Sekelsky J. Detecting de novo mitochondrial mutations in angiosperms with highly divergent evolutionary rates. Genetics. 2021;218(1):iyab039.
pubmed: 33704433 pmcid: 8128415 doi: 10.1093/genetics/iyab039
Gatica-Soria LM, Ceriotti LF, Garcia LE, Virginia S-P. Native and foreign mitochondrial and nuclear encoded proteins conform the OXPHOS complexes of a holoparasitic plant. Gene. 2022;817:146176.
pubmed: 35031426 doi: 10.1016/j.gene.2021.146176
Weng M-L, Ruhlman TA, Jansen RK. Plastid–nuclear interaction and accelerated coevolution in plastid ribosomal genes in Geraniaceae. Genome Biol Evol. 2016;8(6):1824–38.
pubmed: 27190001 pmcid: 4943186 doi: 10.1093/gbe/evw115
Zhang J, Ruhlman TA, Sabir JSM, Blazier JC, Weng M-L, Park S, Jansen RK. Coevolution between nuclear-encoded DNA replication, recombination, and repair genes and plastid genome complexity. Genome Biol Evol. 2016;8(3):622–34.
pubmed: 26893456 pmcid: 4824065 doi: 10.1093/gbe/evw033
Xi Z, Wang Y, Bradley RK, Sugumaran M, Marx CJ, Rest JS, et al. Massive mitochondrial gene transfer in a parasitic flowering plant clade. PLoS Genet. 2013;9(2): e1003265.
pubmed: 23459037 pmcid: 3573108 doi: 10.1371/journal.pgen.1003265
Cai L, Arnold BJ, Xi Z, Khost DE, Patel N, Hartmann CB, et al. Deeply altered genome architecture in the endoparasitic flowering plant Sapria himalayana Griff. (Rafflesiaceae). Curr Biol. 2021;31(5):1–10.
doi: 10.1016/j.cub.2020.12.045
Li M, Liu K, Li Z, Lu H-C, Ye Q, Zhang D, et al. Genomes of leafy and leafless Platanthera orchids illuminate the evolution of mycoheterotrophy. Nat Plants. 2022;8(4):373–88. https://doi.org/10.1038/s41477-022-01127-9 .
doi: 10.1038/s41477-022-01127-9 pubmed: 35449401 pmcid: 9023349
Welsch R, Zhou X, Yuan H, Álvarez D, Sun T, Schlossarek D, et al. Clp protease and or directly control the proteostasis of phytoene synthase, the crucial enzyme for carotenoid biosynthesis in Arabidopsis. Mol Plant. 2018;11(1):149–62.
pubmed: 29155321 doi: 10.1016/j.molp.2017.11.003
Dorrell RG, Azuma T, Nomura M, de Kerdrel GA, Paoli L, Yang S, et al. Principles of plastid reductive evolution illuminated by nonphotosynthetic chrysophytes. Proc Natl Acad Sci USA. 2019;116(14):6914–23.
pubmed: 30872488 pmcid: 6452693 doi: 10.1073/pnas.1819976116
Rowland E, Kim J, Friso G, Poliakov A, Ponnala L, Sun Q, et al. The CLP and PREP protease systems coordinate maturation and degradation of the chloroplast proteome in Arabidopsis thaliana. New Phytol. 2022;236(4):1339–57.
pubmed: 35946374 doi: 10.1111/nph.18426
Sanchez-Puerta MV, Ceriotti LF, Gatica-Soria LM, Roulet ME, Garcia LE, Sato HA. Invited review beyond parasitic convergence: unravelling the evolution of the organellar genomes in holoparasites. Ann Bot. 2023;132(5):909–28.
pubmed: 37503831 pmcid: 10808021 doi: 10.1093/aob/mcad108
Guisinger MM, Kuehl JV, Boore JL, Jansen RK. Genome-wide analyses of Geraniaceae plastid DNA reveal unprecedented patterns of increased nucleotide substitutions. Proc Natl Acad Sci USA. 2008;105(47):18424–9.
pubmed: 19011103 pmcid: 2587588 doi: 10.1073/pnas.0806759105
Sun Y, Deng T, Zhang A, Moore MJ, Landis JB, Lin N, et al. Genome sequencing of the endangered Kingdonia uniflora (Circaeasteraceae, Ranunculales) reveals potential mechanisms of evolutionary specialization. iScience. 2020;23(5):101124.
pubmed: 32428861 pmcid: 7232092 doi: 10.1016/j.isci.2020.101124
Havird JC, Whitehill NS, Snow CD, Sloan DB. Conservative and compensatory evolution in oxidative phosphorylation complexes of angiosperms with highly divergent rates of mitochondrial genome evolution. Evolution. 2015;69(12):3069–81.
pubmed: 26514987 pmcid: 4715514 doi: 10.1111/evo.12808
Jakovlić I, Zou H, Ye T, Zhang H, Liu X, Xiang C-Y, et al. Mitogenomic evolutionary rates in bilateria are influenced by parasitic lifestyle and locomotory capacity. Nat Commun. 2023;14(1):6307.
pubmed: 37813879 pmcid: 10562372 doi: 10.1038/s41467-023-42095-8
Jiang Y, Hu X, Yuan Y, Guo X, Chase MW, Ge S, et al. The Gastrodia menghaiensis (Orchidaceae) genome provides new insights of orchid mycorrhizal interactions. BMC Plant Biol. 2022;22(1):179. https://doi.org/10.1186/s12870-022-03573-1 .
doi: 10.1186/s12870-022-03573-1 pubmed: 35392808 pmcid: 8988336
Xu Y, Lei Y, Su Z, Zhao M, Zhang J, Shen G, et al. A chromosome-scale Gastrodia elata genome and large-scale comparative genomic analysis indicate convergent evolution by gene loss in mycoheterotrophic and parasitic plants. Plant J. 2021;108(6):1609–23 https://onlinelibrary.wiley.com/doi/10.1111/tpj.15528 .
pubmed: 34647389 doi: 10.1111/tpj.15528
Chen X, Fang D, Xu Y, Duan K, Yoshida S, Yang S, et al. Balanophora genomes display massively convergent evolution with other extreme holoparasites and provide novel insights into parasite–host interactions. Nat Plants. 2023;9(10):1627–42. https://doi.org/10.1038/s41477023-01517-7 .
doi: 10.1038/s41477023-01517-7 pubmed: 37735254
Kafri M, Patena W, Martin L, Wang L, Gomer G, Ergun SL, et al. Systematic identification and characterization of genes in the regulation and biogenesis of photosynthetic machinery. Cell. 2023;186(25):5638–55.
pubmed: 38065083 pmcid: 10760936 doi: 10.1016/j.cell.2023.11.007
Mursidawati S, Wicaksono A, Teixeira da Silva JA. Rafflesia patma Blume flower organs: histology of the epidermis and vascular structures, and a search for stomata. Planta. 2020;251(6):112.
pubmed: 32494866 doi: 10.1007/s00425-020-03402-5
Chen C, Wu Y, Li J, Wang X, Zeng Z, Xu J, Liu Y, Feng J, Chen H, He Y, et al. TBtools-II: A “one for all, all for one” bioinformatics platform for biological big-data mining. Mol Plant. 2023;16(11):1733–42.
pubmed: 37740491 doi: 10.1016/j.molp.2023.09.010
Duarte JM, Wall PK, Edger PP, Landherr LL, Ma H, Pires PK, et al. Identification of shared single copy nuclear genes in Arabidopsis, Populus, Vitis and Oryza and their phylogenetic utility across various taxonomic levels. BMC Evol Biol. 2010;10(1): 61.
pubmed: 20181251 pmcid: 2848037 doi: 10.1186/1471-2148-10-61
Katoh K, Standley DM. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol. 2013;30(4):772–80.
pubmed: 23329690 pmcid: 3603318 doi: 10.1093/molbev/mst010
Suyama M, Torrents D, Bork P. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res. 2006;34:W609–12.
pubmed: 16845082 pmcid: 1538804 doi: 10.1093/nar/gkl315
Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25(15):1972–3.
pubmed: 19505945 pmcid: 2712344 doi: 10.1093/bioinformatics/btp348
Emms DM, Kelly S. OrthoFinder: solving fundamental biases in whole genome comparisons dramatically improves orthogroup inference accuracy. Genome Biol. 2015;16(1):157.
pubmed: 26243257 pmcid: 4531804 doi: 10.1186/s13059-015-0721-2
Edgar RC. MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinformatics. 2004;5(1): 113.
pubmed: 15318951 pmcid: 517706 doi: 10.1186/1471-2105-5-113
Zhang D, Gao F, Jakovlić I, Zou H, Zhang J, Li WX, et al. PhyloSuite: An integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol Ecol Resour. 2019;20(1):348–55.
pubmed: 31599058 doi: 10.1111/1755-0998.13096
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37(5):1530–4.
pubmed: 32011700 pmcid: 7182206 doi: 10.1093/molbev/msaa015
Stamatakis A. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics. 2014;30(9):1312–3.
pubmed: 24451623 pmcid: 3998144 doi: 10.1093/bioinformatics/btu033
Yang Z. PAML 4: Phylogenetic analysis by maximum likelihood. Mol Biol Evol. 2007;24(8):1586–91.
pubmed: 17483113 doi: 10.1093/molbev/msm088
Forsythe ES, Williams AM, Sloan DB. Genome-wide signatures of plastid-nuclear coevolution point to repeated perturbations of plastid proteostasis systems across angiosperms. Plant Cell. 2021;33(4):980–97.
pubmed: 33764472 pmcid: 8226287 doi: 10.1093/plcell/koab021
Lohse M, Nagel A, Herter T, May P, Schroda M, Zrenner R, et al. Mercator: a fast and simple web server for genome scale functional annotation of plant sequence data. Plant Cell Environ. 2013;37(5):1250–8.
pubmed: 24237261 doi: 10.1111/pce.12231
Peden JF. Analysis of codon usage. UK: PhD Thesis, University of Nottingham; 1999.

Auteurs

Xuelian Guo (X)

State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China.

Hanchen Wang (H)

State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China.

Dongliang Lin (D)

State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China.

Yajun Wang (Y)

State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China.

Xiaohua Jin (X)

State Key Laboratory of Plant Diversity and Specialty Crops & Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences (IBCAS), Beijing, 100093, China. xiaohuajin@ibcas.ac.cn.

Articles similaires

The landscape of sequence variations between resistant and susceptible hot peppers to predict functional candidate genes against bacterial wilt disease.

Ji-Su Kwon, Junesung Lee, Jayabalan Shilpha et al.
1.00
Capsicum Disease Resistance Plant Diseases Polymorphism, Single Nucleotide Ralstonia solanacearum

Exploring the complexity of genome size reduction in angiosperms.

Akihiro Ezoe, Motoaki Seki
1.00
Genome Size Genome, Plant Magnoliopsida Evolution, Molecular Arabidopsis

Comparative analysis of chloroplast genomes in ten holly (Ilex) species: insights into phylogenetics and genome evolution.

Jiaxin Hu, Daoliang Yan, Huwei Yuan et al.
1.00
Genome, Chloroplast Phylogeny Evolution, Molecular Ilex Microsatellite Repeats

Comparative analysis of the PAL gene family in nine citruses provides new insights into the stress resistance mechanism of Citrus species.

Tuo Yin, Rong Xu, Ling Zhu et al.
1.00
Citrus Phenylalanine Ammonia-Lyase Stress, Physiological Multigene Family Phylogeny

Classifications MeSH

questionsmedicales.fr › Métabolisme › Processus hétérotrophes › Cytonuclear evolution in fully heterotrophic...
questionsmedicales.fr › Phénomènes biologiques › Évolution biologique › Évolution moléculaire › Cytonuclear evolution in fully heterotrophic...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Noyau de la cellule › Cytonuclear evolution in fully heterotrophic...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Génome › Génome végétal › Gènes de plante › Cytonuclear evolution in fully heterotrophic...
questionsmedicales.fr › Cellules › Structures cellulaires › Espace intracellulaire › Cytoplasme › Structures cytoplasmiques › Organites › Plastes › Cytonuclear evolution in fully heterotrophic...