Polyploidy and subsequent post-polyploid diploidization (PPD) are key drivers of plant genome evolution, yet their contributions to evolutionary success remain debated. Here, we analyze the Malvaceae family as an exemplary system for elucidating the evolutionary role of polyploidy and PPD in angiosperms, leveraging 11 high-quality chromosome-scale genomes from all nine subfamilies, including newly sequenced, near telomere-to-telomere assemblies from four of these subfamilies. Our findings reveal a complex reticulate paleoallopolyploidy history early in the diversification of the Malvadendrina clade, characterized by multiple rounds of species radiation punctuated by ancient allotetraploidization (Mal-β) and allodecaploidization (Mal-α) events around the Cretaceous-Paleogene (K-Pg) boundary. We further reconstruct the evolutionary dynamics of PPD and find a strong correlation between dysploidy rate and taxonomic richness of the paleopolyploid subfamilies (R2 ≥ 0.90, P < 1e-4), supporting the "polyploidy for survival and PPD for success" hypothesis. Overall, our study provides a comprehensive reconstruction of the evolutionary history of the Malvaceae and underscores the crucial role of polyploidy-dysploidy waves in shaping plant biodiversity.

CAS Key Laboratory of Tropical Forest Ecology Xishuangbanna Tropical Botanical Garden Chinese Academy of Sciences Mengla 666303 China

CEITEC Central European Institute of Technology and Department of Experimental Botany Faculty of Science Masaryk University Brno CZ 625 00 Czech Republic

College of Life Sciences Qufu Normal University Qufu 273165 China

Department of Ecology Evolution and Organismal Biology Iowa State University Amees IA 50011 USA

Donald Danforth Plant Science Center St Louis MO 63132 USA

Ecology and Evolutionary Biology Department Molecular and Cellular Biology Department University of Arizona Tucson AZ 85718 USA

Institute of Crop Germplasm Resources Shandong Academy of Agricultural Sciences Jinan 250100 China

State Key Laboratory of Cotton Biology Institute of Cotton Research Chinese Academy of Agricultural Sciences Anyang 455000 China

University of Chinese Academy of Sciences Beijing 101408 China

Wuhan Botanical Garden Chinese Academy of Sciences Wuhan 430074 China

Yunnan Key Laboratory for Integrative Conservation of Plant Species with Extremely Small Populations State Key Laboratory of Plant Diversity and Specialty Crops Kunming Institute of Botany Chinese Academy of Sciences Kunming 650201 China

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Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. PubMed

Jiao, Y. et al. Ancestral polyploidy in seed plants and angiosperms. PubMed

Cheng, F. et al. Gene retention, fractionation and subgenome differences in polyploid plants. PubMed

Zhang, R. G. et al. Subgenome-aware analyses suggest a reticulate allopolyploidization origin in three PubMed PMC

Zhang, R. G., Shang, H., Jia, K. & Ma, Y. Subgenome phasing for complex allopolyploidy: case-based benchmarking and recommendations. PubMed PMC

Stull, G. W., Pham, K. K., Soltis, P. S. & Soltis, D. E. Deep reticulation: the long legacy of hybridization in vascular plant evolution. PubMed

Bapteste, E. et al. Networks: expanding evolutionary thinking. PubMed

Ma, P. F. et al. Genome assemblies of 11 bamboo species highlight diversification induced by dynamic subgenome dominance. PubMed PMC

Fawcett, J. A., Maere, S. & van de Peer, Y. Plants with double genomes might have had a better chance to survive the Cretaceous-Tertiary extinction event. PubMed PMC

Zhang, L. et al. The ancient wave of polyploidization events in flowering plants and their facilitated adaptation to environmental stress. PubMed

Ebadi, M. et al. The duplication of genomes and genetic networks and its potential for evolutionary adaptation and survival during environmental turmoil. PubMed PMC

Román-Palacios, C., Molina-Henao, Y. F. & Barker, M. S. Polyploids increase overall diversity despite higher turnover than diploids in the Brassicaceae. PubMed PMC

Schranz, M. E., Mohammadin, S. & Edger, P. P. Ancient whole genome duplications, novelty and diversification: the WGD Radiation Lag-Time Model. PubMed

Tank, D. C. et al. Nested radiations and the pulse of angiosperm diversification: increased diversification rates often follow whole genome duplications. PubMed

Heslop-Harrison, J. S. P., Schwarzacher, T. & Liu, Q. Polyploidy: its consequences and enabling role in plant diversification and evolution. PubMed PMC

Soltis, P. S. & Soltis, D. E. Ancient WGD events as drivers of key innovations in angiosperms. PubMed

Scarpino, S. V., Levin, D. A. & Meyers, L. A. Polyploid formation shapes flowering plant diversity. PubMed

Mayrose, I. et al. Recently formed polyploid plants diversify at lower rates. PubMed

Arrigo, N. & Barker, M. S. Rarely successful polyploids and their legacy in plant genomes. PubMed

Vamosi, J. C., Magallon, S., Mayrose, I., Otto, S. P. & Sauquet, H. Macroevolutionary patterns of flowering plant speciation and extinction. PubMed

Dodsworth, S., Chase, M. W. & Leitch, A. R. Is post-polyploidization diploidization the key to the evolutionary success of angiosperms?

Mandáková, T. & Lysak, M. A. Post-polyploid diploidization and diversification through dysploid changes. PubMed

Alverson, W. S., Whitlock, B. A., Nyffeler, R., Bayer, C. & Baum, D. A. Phylogeny of the core Malvales: evidence from PubMed

Bayer, C. et al. Support for an expanded family concept of Malvaceae within a recircumscribed order Malvales: a combined analysis of plastid

Baum, D. A., Alverson, W. S. & Nyffeler, R. A durian by any other name: taxonomy and nomenclature of the core Malvales.

Baum, D. A. et al. Phylogenetic relationships of Malvatheca (Bombacoideae and Malvoideae; Malvaceae sensu lato) as inferred from plastid DNA sequences. PubMed

Cvetkovic, T. et al. Phylogenomics resolves deep subfamilial relationships in Malvaceae s.l. PubMed PMC

Hernández-Gutiérrez, R., Mendoza, C. G. & Magallón, S. Low-copy nuclear genes reveal new evidence of incongruence in relationships within Malvaceae s.l.

Hernández-Gutiérrez, R. et al. Localized phylogenetic discordance among nuclear loci due to incomplete lineage sorting and introgression in the family of cotton and cacao (Malvaceae). PubMed PMC

Hernández-Gutiérrez, R. & Magallón, S. The timing of Malvales evolution: Incorporating its extensive fossil record to inform about lineage diversification. PubMed

Nyffeler, R. et al. Phylogenetic analysis of the Malvadendrina clade (Malvaceae s.l.) based on plastid DNA sequences.

Wang, J., Moore, M. J., Wang, H., Zhu, Z. & Wang, H. Plastome evolution and phylogenetic relationships among Malvaceae subfamilies. PubMed

Conover, J. L. et al. A Malvaceae mystery: a mallow maelstrom of genome multiplications and maybe misleading methods? PubMed

Paterson, A. H. et al. Repeated polyploidization of PubMed

Wang, X. et al. Comparative genomic de-convolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation. PubMed

Teh, B. T. et al. The draft genome of tropical fruit durian ( PubMed

Wang, J. et al. Recursive paleohexaploidization shapes the durian genome. PubMed PMC

Sun, P. et al. Subgenome-aware analyses reveal the genomic consequences of ancient allopolyploid hybridizations throughout the cotton family. PubMed PMC

Mapleson, D., Garcia Accinelli, G., Kettleborough, G., Wright, J. & Clavijo, B. J. KAT: a K-mer analysis toolkit to quality control NGS datasets and genome assemblies. PubMed PMC

Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V. & Zdobnov, E. M. BUSCO: assessing genome assembly and annotation completeness with single-copy orthologs. PubMed

Liu, D., Tian, X., Shao, S., Ma, Y. & Zhang, R. Haplotype-resolved chromosomal-level genome assembly of Buzhaye ( PubMed PMC

Motamayor, J. C. et al. The genome sequence of the most widely cultivated cacao type and its use to identify candidate genes regulating pod color. PubMed PMC

Yang, J., Zhang, R., Ma, Y., Ma, Y. & Sun, W. Genome assembly of

Sahu, S. K. et al. Chromosome-scale genomes of commercial timber trees ( PubMed PMC

Yuan, G. et al. A telomere-to-telomere reference genome assembly of the red silk cotton tree ( PubMed PMC

Zhang, R. G. et al. SOI: robust identification of orthologous synteny with the PubMed PMC

Argout, X. et al. The genome of PubMed

Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. PubMed

Shao, L. et al. High-quality genomes of PubMed PMC

Marcussen, T. et al. Ancient hybridizations among the ancestral genomes of bread wheat. PubMed

He, Q. et al. High-quality genome of allotetraploid PubMed PMC

Guo, X. et al. Linked by ancestral bonds: multiple whole-genome duplications and reticulate evolution in a Brassicaceae tribe. PubMed PMC

Jang, T. et al. Multiple origins and nested cycles of hybridization result in high tetraploid diversity in the monocot PubMed PMC

Steenwyk, J. L., Li, Y., Zhou, X., Shen, X. & Rokas, A. Incongruence in the phylogenomics era. PubMed PMC

Nyffeler, R. & Baum, D. A. Phylogenetic relationships of the durians (Bombacaceae-Durioneae or /Malvaceae/Helicteroideae/Durioneae) based on chloroplast and nuclear ribosomal DNA sequences.

Degnan, J. & Rosenberg, N. Gene tree discordance, phylogenetic inference and the multispecies coalescent. PubMed

Sun, P. et al. WGDI: A user-friendly toolkit for evolutionary analyses of whole-genome duplications and ancestral karyotypes. PubMed

Sun, P. et al. Whole-genome-based paloegenomics reveals angiosperm karyotype evolution during their early history. 10.2139/ssrn.4482425 (2023).

Udall, J. A. et al. The genome sequence of PubMed PMC

Wang, M. et al. Genomic innovation and regulatory rewiring during evolution of the cotton genus PubMed

Marinho, R. C. et al. Do chromosome numbers reflect phylogeny? New counts for Bombacoideae and a review of Malvaceae s.l. PubMed

Feng, X. et al. Genomic evidence for rediploidization and adaptive evolution following the whole-genome triplication. PubMed PMC

Wang, J. et al. Deciphering recursive polyploidization in Lamiales and reconstructing their chromosome evolutionary trajectories. PubMed

Zhang, T. et al. Cultivated hawthorn ( PubMed

Ding, Y. M. et al. Genome structure-based Juglandaceae phylogenies contradict alignment-based phylogenies and substitution rates vary with DNA repair genes. PubMed PMC

Lanfear, R. et al. Taller plants have lower rates of molecular evolution. PubMed

Cheng, F. et al. Biased gene fractionation and dominant gene expression among the subgenomes of PubMed PMC

Brownfield, L. & Kohler, C. Unreduced gamete formation in plants: mechanisms and prospects. PubMed

Garsmeur, O. et al. Two evolutionarily distinct classes of paleopolyploidy. PubMed

Li, Z. et al. Gene duplicability of core genes is highly consistent across all angiosperms. PubMed PMC

Jiang, W., Liu, Y., Xia, E. & Gao, L. Prevalent role of gene features in determining evolutionary fates of whole-genome duplication duplicated genes in flowering plants. PubMed PMC

Chen, H., Almeida-Silva, F., Logghe, G., Bonte, D. & Van de Peer, Y. The rise of polyploids during environmental catastrophes. 10.1101/2024.11.22.624806 (2024).

Soltis, D. E., Buggs, R. J. A., Doyle, J. J. & Soltis, P. S. What we still don’t know about polyploidy.

Comai, L. The advantages and disadvantages of being polyploid. PubMed

Li, Z. et al. Patterns and processes of diploidization in land plants. PubMed

Qian, H. & Jin, Y. An updated megaphylogeny of plants, a tool for generating plant phylogenies and an analysis of phylogenetic community structure.

Ramsey, J. & Schemske, D. W. Neopolyploidy in flowering plants.

Rieseberg, L. H. Chromosomal rearrangements and speciation. PubMed

Bowers, J. E. & Paterson, A. H. Chromosome number is key to longevity of polyploid lineages. PubMed

Carta, A. & Escudero, M. Karyotypic diversity: a neglected trait to explain angiosperm diversification? PubMed

Albalat, R. & Cañestro, C. Evolution by gene loss. PubMed

Xiong, Z., Gaeta, R. T. & Pires, J. C. Homoeologous shuffling and chromosome compensation maintain genome balance in resynthesized allopolyploid PubMed PMC

Chester, M. et al. Extensive chromosomal variation in a recently formed natural allopolyploid species, PubMed PMC

Doyle, J. J. & Doyle, J. L. A rapid DNA isolation procedure from small quantity of fresh leaf material.

van Berkum, N. L. et al. Hi-C: a method to study the three-dimensional architecture of genomes. PubMed PMC

Kokot, M., Długosz, M. & Deorowicz, S. KMC 3: counting and manipulating k-mer statistics. PubMed

Ranallo-Benavidez, T. R., Jaron, K. S. & Schatz, M. C. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. PubMed PMC

Cheng, H., Concepcion, G. T., Feng, X., Zhang, H. & Li, H. Haplotype-resolved de novo assembly using phased assembly graphs with hifiasm. PubMed PMC

Cheng, H. et al. Haplotype-resolved assembly of diploid genomes without parental data. PubMed PMC

Durand, N. C. et al. Juicer provides a one-click system for analyzing loop-eesolution Hi-C experiments. PubMed PMC

Dudchenko, O. et al. De novo assembly of the PubMed PMC

Durand, N. C. et al. Juicebox provides a visualization system for Hi-C contact maps with unlimited zoom. PubMed PMC

Xu, G. et al. LR_Gapcloser: a tiling path-based gap closer that uses long reads to complete genome assembly. PubMed PMC

Adams, S. P. et al. Loss and recovery of PubMed PMC

Jin, J. et al. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. PubMed PMC

Wick, R. R., Schultz, M. B., Zobel, J. & Holt, K. E. Bandage: interactive visualization of de novo genome assemblies. PubMed PMC

Hu, J. et al. NextPolish2: a repeat-aware polishing tool for genomes assembled using HiFi long reads. PubMed PMC

Pryszcz, L. P. & Toni, G. Redundans: an assembly pipeline for highly heterozygous genomes. PubMed PMC

Ou, S. et al. Benchmarking transposable element annotation methods for creation of a streamlined, comprehensive pipeline. PubMed PMC

Tarailo-Graovac, M. & Chen, N. Using RepeatMasker to identify repetitive elements in genomic sequences. PubMed

Zhang, L. et al. Reference genomes of the two cultivated jute species. PubMed PMC

He, Z. et al. Evolution of coastal forests based on a full set of mangrove genomes. PubMed

Gao, Y. et al. De novo genome assembly of the red silk cotton tree ( PubMed PMC

Wang, S. et al. The chromosome-scale genomes of PubMed PMC

Ding, X. et al. Genome sequence of the agarwood tree PubMed PMC

Cheng, C. Y. et al. Araport11: a complete reannotation of the PubMed

Yue, J. et al. SunUp and Sunset genomes revealed impact of particle bombardment mediated transformation and domestication history in papaya. PubMed

Li, H. Minimap2: pairwise alignment for nucleotide sequences. PubMed PMC

Pertea, M. et al. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. PubMed PMC

Haas, B. J. et al. Improving the PubMed PMC

Holt, C. & Yandell, M. MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects. PubMed PMC

Haas, B. J. et al. Automated eukaryotic gene structure annotation using EVidenceModeler and the Program to Assemble Spliced Alignments. PubMed PMC

Zhang, R. G. et al. TEsorter: an accurate and fast method to classify LTR-retrotransposons in plant genomes. PubMed PMC

Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. PubMed PMC

Nawrocki, E. P. et al. Rfam 12.0: updates to the RNA families database. PubMed PMC

Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-mapper. PubMed PMC

Buchfink, B., Xie, C. & Huson, D. H. Fast and sensitive protein alignment using DIAMOND. PubMed

Jones, P. et al. InterProScan 5: genome-scale protein function classification. PubMed PMC

Emms, D. M. & Kelly, S. OrthoFinder: phylogenetic orthology inference for comparative genomics. PubMed PMC

Zhang, C. & Mirarab, S. ASTRAL-Pro 2: ultrafast species tree reconstruction from multi-copy gene family trees. PubMed

Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. PubMed PMC

Standley, D. M. & Katoh, K. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. PubMed PMC

Capella-Gutiérrez, S., Silla-Martínez, J. M. & Gabaldón, T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. PubMed PMC

Wang, Z. et al. A high-quality PubMed PMC

Jia, K. et al. SubPhaser: a robust allopolyploid subgenome phasing method based on subgenome-specific PubMed

Zhang, C., Mirarab, S. & Takahashi, A. Weighting by gene tree uncertainty improves accuracy of quartet-based species trees. PubMed PMC

Zhang, C., Nielsen, R. & Mirarab, S. CASTER: Direct species tree inference from whole-genome alignments. PubMed PMC

Huson, D. H. & Bryant, D. Application of phylogenetic networks in evolutionary studies. PubMed

Kvacek, Z., Manchester, S. R. & Akhmetiev, M. A. Review of the fossil history of

Ferguson, D. K., Liu, Y. S. & Zetter, R. The paleoendemic plants of East Asia: evidence from the fossil record for changing distribution patterns. In: (ed Jablonski, N. G.).

Carvalho, M. R., Herrera, F. A., Jaramillo, C. A., Wing, S. L. & Callejas, R. Paleocene Malvaceae from northern South America and their biogeographical implications. PubMed

Kumar, S. et al. TimeTree 5: an expanded resource for species divergence times. PubMed PMC

Sanderson, M. J. r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. PubMed

Yang, Z. PAML 4: phylogenetic analysis by maximum likelihood. PubMed

Claramunt, S. CladeDate: Calibration information generator for divergence time estimation.

Silvestro, D. et al. Fossil data support a pre-Cretaceous origin of flowering plants. PubMed

Shang, H. et al. Phytop: A tool for visualizing and recognizing signals of incomplete lineage sorting and hybridization using species trees output from ASTRAL. PubMed PMC

Tian, Z. et al. Thirteen Dipterocarpoideae genomes provide insights into their evolution and borneol biosynthesis. PubMed PMC

Solís-Lemus, C. & Ané, C. Inferring phylogenetic networks with maximum pseudolikelihood under incomplete lineage sorting. PubMed PMC

Solís-Lemus, C., Bastide, P. & Ané, C. PhyloNetworks: a package for phylogenetic networks. PubMed

Cai, R. & Ané, C. Assessing the fit of the multi-species network coalescent to multi-locus data. PubMed

Pang, X. & Zhang, D. Detection of ghost introgression requires exploiting topological and branch length information. PubMed PMC

Flouri, T., Jiao, X., Rannala, B. & Yang, Z. A Bayesian implementation of the multispecies coalescent model with introgression for phylogenomic analysis. PubMed PMC

Rannala, B. & Yang, Z. Efficient Bayesian species tree inference under the multispecies coalescent. PubMed PMC

Flouri, T. et al. Bayesian phylogenetic inference using relaxed-clocks and the multispecies coalescent. PubMed PMC

Chen, S., Zhou, Y., Chen, Y. & Gu, J. fastp: an ultra-fast all-in-one FASTQ preprocessor. PubMed PMC

Kim, D., Langmead, B. & Salzberg, S. L. HISAT: a fast spliced aligner with low memory requirements. PubMed PMC

Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. PubMed PMC

Young, M. D., Wakefield, M. J., Smyth, G. K. & Oshlack, A. Gene ontology analysis for RNA-seq: accounting for selection bias. PubMed PMC

Kindt, R. WorldFlora: An R package for exact and fuzzy matching of plant names against the World Flora Online taxonomic backbone data. PubMed PMC

Kattge, J. et al. TRY plant trait database – enhanced coverage and open access. PubMed

Delgado-Paredes, G. E. et al. In situ germplasm conservation of

Idowu, B. F. & Samuel, O. A. Cacao growth and development under different nursery and field conditions. In: (ed Peter, O. A.).

Paradis, E. & Schliep, K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. PubMed