Soltis, D. E. et al. Polyploidy and angiosperm diversification. Am. J. Bot. 96, 336–348 (2009).
Van de Peer, Y., Mizrachi, E. & Marchal, K. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411–424 (2017).
Amborella Genome Project et al. The Amborella genome and the evolution of flowering plants. Science 342, 1241089 (2013).
Chanderbali, A. S. et al. Buxus and Tetracentron genomes help resolve eudicot genome history. Nat. Commun. 13, 643 (2022).
Dehal, P. & Boore, J. L. Two rounds of whole genome duplication in the ancestral vertebrate. PLoS Biol. 3, e314 (2005).
Edger, P. P. et al. Subgenome dominance in an interspecific hybrid, synthetic allopolyploid, and a 140-year-old naturally established neo-allopolyploid monkeyflower. Plant Cell 29, 2150–2167 (2017).
Li, Z. et al. Patterns and processes of diploidization in land plants. Annu. Rev. Plant Biol. 72, 387–410 (2021).
Cheng, F. et al. Gene retention, fractionation and subgenome differences in polyploid plants. Nat. Plants 4, 258–268 (2018).
Cross, A. T., Krueger, T. A., Gonella, P. M., Robinson, A. S. & Fleischmann, A. S. Conservation of carnivorous plants in the age of extinction. Glob. Ecol. Conserv. 24, e01272 (2020).
Ellison, A. M. & Adamec, L. R. (eds) Carnivorous Plants: Physiology, Ecology, and Evolution (Oxford Univ. Press, 2018).
Renner, S. S. & Ricklefs, R. E. Dioecy and its correlates in the flowering plants. Am. J. Bot. 82, 596–606 (1995).
Walker, J. F. et al. Widespread paleopolyploidy, gene tree conflict, and recalcitrant relationships among the carnivorous Caryophyllales. Am. J. Bot. 104, 858–867 (2017).
Yang, Y. et al. Improved transcriptome sampling pinpoints 26 ancient and more recent polyploidy events in Caryophyllales, including two allopolyploidy events. New Phytol. 217, 855–870 (2018).
Palfalvi, G. et al. Genomes of the Venus flytrap and close relatives unveil the roots of plant carnivory. Curr. Biol. 30, 2312–2320.e5 (2020).
Heubl, G. & Wistuba, A. A cytological study of the genus Nepenthes L. (Nepenthaceae). Sendtnera 4, 169–174 (1997).
Manni, M., Berkeley, M. R., Seppey, M., Simão, F. A. & Zdobnov, E. M. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol. Biol. Evol. 38, 4647–4654 (2021).
Minh, B. Q. et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530–1534 (2020).
Zhang, C., Rabiee, M., Sayyari, E. & Mirarab, S. ASTRAL-III: polynomial time species tree reconstruction from partially resolved gene trees. BMC Bioinform. 19, 153 (2018).
Albert, V. A., Williams, S. E. & Chase, M. W. Carnivorous plants: phylogeny and structural evolution. Science 257, 1491–1495 (1992).
Heubl, G., Bringmann, G. & Meimberg, H. Molecular phylogeny and character evolution of carnivorous plant families in Caryophyllales—revisited. Plant Biol. 8, 821–830 (2006).
Freund, M. et al. The digestive systems of carnivorous plants. Plant Physiol. 190, 44–59 (2022).
Barrett, S. C. H., Yakimowski, S. B., Field, D. L. & Pickup, M. Ecological genetics of sex ratios in plant populations. Philos. Trans. R. Soc. B 365, 2549–2557 (2010).
Scharmann, M., Grafe, T. U., Metali, F. & Widmer, A. Sex is determined by XY chromosomes across the radiation of dioecious Nepenthes pitcher plants. Evol. Lett. 3, 586–597 (2019).
Jaillon, O. et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449, 463–467 (2007).
Scharmann, M., Wistuba, A. & Widmer, A. Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants. Mol. Phylogenet. Evol. 163, 107214 (2021).
Joyce, B. L. et al. FractBias: a graphical tool for assessing fractionation bias following polyploidy. Bioinformatics 33, 552–554 (2017).
Yu, Z., Zheng, C., Albert, V. A. & Sankoff, D. Excision dominates pseudogenization during fractionation after whole genome duplication and in gene loss after speciation in plants. Front. Genet. 11, 603056 (2020).
Alger, E. I. & Edger, P. P. One subgenome to rule them all: underlying mechanisms of subgenome dominance. Curr. Opin. Plant Biol. 54, 108–113 (2020).
Jia, K.-H. et al. SubPhaser: a robust allopolyploid subgenome phasing method based on subgenome-specific k-mers. New Phytol. 235, 801–809 (2022).
Wang, X. et al. Comparative genomic de-convolution of the cotton genome revealed a decaploid ancestor and widespread chromosomal fractionation. New Phytol. 209, 1252–1263 (2016).
Ashman, T.-L. et al. Tree of sex: a database of sexual systems. Sci. Data 1, 140015 (2014).
Harkess, A. et al. Sex determination by two Y-linked genes in garden asparagus. Plant Cell 32, 1790–1796 (2020).
Schwander, T., Libbrecht, R. & Keller, L. Supergenes and complex phenotypes. Curr. Biol. 24, R288–R294 (2014).
Li, J. et al. Integration of genetic and physical maps of the Primula vulgaris S locus and localization by chromosome in situ hybridization. New Phytol. 208, 137–148 (2015).
Rifkin, J. L. et al. Widespread recombination suppression facilitates plant sex chromosome evolution. Mol. Biol. Evol. 38, 1018–1030 (2021).
Potente, G. et al. Comparative genomics elucidates the origin of a supergene controlling floral heteromorphism. Mol. Biol. Evol. 39, msac035 (2022).
Akagi, T. et al. Recurrent neo-sex chromosome evolution in kiwifruit. Nat. Plants 9, 393–402 (2023).
Horiuchi, A. et al. Ongoing rapid evolution of a post-Y region revealed by chromosome-scale genome assembly of a hexaploid monoecious persimmon (Diospyros kaki). Mol. Biol. Evol. 40, msad151 (2023).
Yue, J. et al. The origin and evolution of sex chromosomes, revealed by sequencing of the Silene latifolia female genome. Curr. Biol. 33, 2504–2514.e3 (2023).
Westergaard, M. The mechanism of sex determination in dioecious flowering plants. in Advances in Genetics Vol. 9 (ed. Demerec, M.) 217–281 (Academic, 1958).
Charlesworth, B. & Charlesworth, D. A model for the evolution of dioecy and gynodioecy. Am. Nat. 112, 975–997 (1978).
Zhang, W. et al. Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development 133, 3085–3095 (2006).
Zhu, J. et al. Defective in Tapetal Development and Function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55, 266–277 (2008).
Murase, K. et al. MYB transcription factor gene involved in sex determination in Asparagus officinalis. Genes Cells 22, 115–123 (2017).
Yang, X., Makaroff, C. A. & Ma, H. The Arabidopsis MALE MEIOCYTE DEATH1 gene encodes a PHD-finger protein that is required for male meiosis. Plant Cell 15, 1281–1295 (2003).
Subramanyam, K. & Narayana, L. L. A contribution to the floral anatomy of Nepenthes khasiana Hook F. Proc. Indian Acad. Sci. 73, 124–131 (1971).
Moyroud, E., Kusters, E., Monniaux, M., Koes, R. & Parcy, F. LEAFY blossoms. Trends Plant Sci. 15, 346–352 (2010).
Moyroud, E., Tichtinsky, G. & Parcy, F. The LEAFY floral regulators in angiosperms: conserved proteins with diverse roles. J. Plant Biol. 52, 177–185 (2009).
Castro-Mondragon, J. A. et al. JASPAR 2022: the 9th release of the open-access database of transcription factor binding profiles. Nucleic Acids Res. 50, D165–D173 (2022).
Liu, J. et al. Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. Proc. Natl Acad. Sci. USA 112, E5123–E5132 (2015).
Honma, T. & Goto, K. The Arabidopsis floral homeotic gene PISTILLATA is regulated by discrete cis-elements responsive to induction and maintenance signals. Development 127, 2021–2030 (2000).
Theißen, G., Melzer, R. & Rümpler, F. MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143, 3259–3271 (2016).
Sather, D. N., Jovanovic, M. & Golenberg, E. M. Functional analysis of B and C class floral organ genes in spinach demonstrates their role in sexual dimorphism. BMC Plant Biol. 10, 46 (2010).
Tsukaya, H. Comparative leaf development in angiosperms. Curr. Opin. Plant Biol. 17, 103–109 (2014).
Renner, T. & Specht, C. D. A sticky situation: assessing adaptations for plant carnivory in the Caryophyllales by means of stochastic character mapping. Int. J. Plant Sci. 172, 889–901 (2011).
Bemm, F. et al. Venus flytrap carnivorous lifestyle builds on herbivore defense strategies. Genome Res. 26, 1–14 (2016).
Iosip, A. L. et al. The Venus flytrap trigger hair-specific potassium channel KDM1 can reestablish the K+ gradient required for hapto-electric signaling. PLoS Biol. 18, e3000964 (2020).
Procko, C. et al. Stretch-activated ion channels identified in the touch-sensitive structures of carnivorous Droseraceae plants. eLife 10, e64250 (2021).
Klepikova, A. V., Kasianov, A. S., Gerasimov, E. S., Logacheva, M. D. & Penin, A. A. A high resolution map of the Arabidopsis thaliana developmental transcriptome based on RNA-seq profiling. Plant J. 88, 1058–1070 (2016).
Robinson, M. D. & Oshlack, A. A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol. 11, 2010–2011 (2010).
Pavlovič, A., Masarovičová, E. & Hudák, J. Carnivorous syndrome in Asian pitcher plants of the genus Nepenthes. Ann. Bot. 100, 527–536 (2007).
Pavlovič, A. Photosynthetic characterization of Australian pitcher plant Cephalotus follicularis. Photosynthetica 49, 253–258 (2011).
Yilamujiang, A., Reichelt, M. & Mithöfer, A. Slow food: insect prey and chitin induce phytohormone accumulation and gene expression in carnivorous Nepenthes plants. Ann. Bot. 118, 369–375 (2016).
Glazebrook, J. Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu. Rev. Phytopathol. 43, 205–227 (2005).
Erb, M., Meldau, S. & Howe, G. A. Role of phytohormones in insect-specific plant reactions. Trends Plant Sci. 17, 250–259 (2012).
Pavlovič, A. & Mithöfer, A. Jasmonate signalling in carnivorous plants: copycat of plant defence mechanisms. J. Exp. Bot. 70, 3379–3389 (2019).
Capó-Bauçà, S., Font-Carrascosa, M., Ribas-Carbó, M., Pavlovič, A. & Galmés, J. Biochemical and mesophyll diffusional limits to photosynthesis are determined by prey and root nutrient uptake in the carnivorous pitcher plant Nepenthes × ventrata. Ann. Bot. 126, 25–37 (2020).
Durand, D. & Hoberman, R. Diagnosing duplications—can it be done? Trends Genet. 22, 156–164 (2006).
Yanai, I. et al. Genome-wide midrange transcription profiles reveal expression level relationships in human tissue specification. Bioinformatics 21, 650–659 (2005).
Kryuchkova-Mostacci, N. & Robinson-Rechavi, M. A benchmark of gene expression tissue-specificity metrics. Brief. Bioinform. 44, bbw008 (2016).
Callard, D., Axelos, M. & Mazzolini, L. Novel molecular markers for late phases of the growth cycle of Arabidopsis thaliana cell-suspension cultures are expressed during organ senescence. Plant Physiol. 112, 705–715 (1996).
Lee, K., Zawadzka, A., Czarnocki, Z., Reiter, R. J. & Back, K. Molecular cloning of melatonin 3-hydroxylase and its production of cyclic 3-hydroxymelatonin in rice (Oryza sativa). J. Pineal Res. 61, 470–478 (2016).
Choi, G.-H. & Back, K. Cyclic 3-hydroxymelatonin exhibits diurnal rhythm and cyclic 3-hydroxymelatonin overproduction increases secondary tillers in rice by upregulating MOC1 expression. Melatonin Res. 2, 120–138 (2019).
Lee, H. Y. & Back, K. The antioxidant cyclic 3-hydroxymelatonin promotes the growth and flowering of Arabidopsis thaliana. Antioxidants 11, 1157 (2022).
Chia, T. F., Aung, H. H., Osipov, A. N., Goh, N. K. & Chia, L. S. Carnivorous pitcher plant uses free radicals in the digestion of prey. Redox Rep. 9, 255–261 (2004).
Hatano, N. & Hamada, T. Proteomic analysis of secreted protein induced by a component of prey in pitcher fluid of the carnivorous plant Nepenthes alata. J. Proteomics 75, 4844–4852 (2012).
Fukushima, K. et al. Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. Nat. Ecol. Evol. 1, 0059 (2017).
Wal, A., Staszek, P., Pakula, B., Paradowska, M. & Krasuska, U. ROS and RNS alterations in the digestive fluid of Nepenthes × ventrata trap at different developmental stages. Plants 11, 3304 (2022).
Buchfink, B., Reuter, K. & Drost, H.-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021).
Freeling, M. Bias in plant gene content following different sorts of duplication: tandem, whole-genome, segmental, or by transposition. Annu. Rev. Plant Biol. 60, 433–453 (2009).
Conant, G. C. & Wolfe, K. H. Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9, 938–950 (2008).
Hedrich, R. & Fukushima, K. On the origin of carnivory: molecular physiology and evolution of plants on an animal diet. Annu. Rev. Plant Biol. 72, 133–153 (2021).
Pannell, J. R. & Jordan, C. Y. Evolutionary transitions between hermaphroditism and dioecy in animals and plants. Annu. Rev. Ecol. Evol. Syst. 53, 183–201 (2022).
Cronk, Q. & Müller, N. A. Default sex and single gene sex determination in dioecious plants. Front. Plant Sci. 11, 1162 (2020).
Renner, S. S. & Müller, N. A. Plant sex chromosomes defy evolutionary models of expanding recombination suppression and genetic degeneration. Nat. Plants 7, 392–402 (2021).
Albert, V. A., Oppenheimer, D. G. & Lindqvist, C. Pleiotropy, redundancy and the evolution of flowers. Trends Plant Sci. 7, 297–301 (2002).
Bringmann, G., Rischer, H., Schlauer, J. & Aké Assi, L. In vitro propagation of Ancistrocladus abbreviatus Airy Shaw (Ancistrocladaceae). Plant Cell Tissue Organ Cult. 57, 71–73 (1999).
Fukushima, K., Narukawa, H., Palfalvi, G. & Hasebe, M. A discordance of seasonally covarying cues uncovers misregulated phenotypes in the heterophyllous pitcher plant Cephalotus follicularis. Proc. R. Soc. B 288, 20202568 (2021).
Bringmann, G., Rübenacker, M., Jansen, J. R., Scheutzow, D. & Aké Assi, L. On the structure of the Dioncophyllaceae alkaloids dioncophylline A (‘triphyophylline’) and ‘O-methyl-triphyophylline’. Tetrahedron Lett. 31, 639–642 (1990).
Bringmann, G. & Rischer, H. In vitro propagation of the alkaloid-producing rare African liana, Triphyophyllum peltatum (Dioncophyllaceae). Plant Cell Rep. 20, 591–595 (2001).
Murashige, T. & Skoog, F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plant. 15, 473–497 (1962).
Michael, T. P. et al. High contiguity Arabidopsis thaliana genome assembly with a single nanopore flow cell. Nat. Commun. 9, 541 (2018).
Putnam, N. H. et al. Chromosome-scale shotgun assembly using an in vitro method for long-range linkage. Genome Res. 26, 342–350 (2016).
Haug-Baltzell, A., Stephens, S. A., Davey, S., Scheidegger, C. E. & Lyons, E. SynMap2 and SynMap3D: web-based whole-genome synteny browsers. Bioinformatics 33, 2197–2198 (2017).
Novák, P., Neumann, P. & Macas, J. Global analysis of repetitive DNA from unassembled sequence reads using RepeatExplorer2. Nat. Protoc. 15, 3745–3776 (2020).
Neumann, P., Novák, P., Hoštáková, N. & Macas, J. Systematic survey of plant LTR-retrotransposons elucidates phylogenetic relationships of their polyprotein domains and provides a reference for element classification. Mob. DNA 10, 1 (2019).
Lopez-Delisle, L. et al. pyGenomeTracks: reproducible plots for multivariate genomic datasets. Bioinformatics 37, 422–423 (2021).
Brůna, T., Lomsadze, A. & Borodovsky, M. GeneMark-EP+: eukaryotic gene prediction with self-training in the space of genes and proteins. NAR Genom. Bioinform. 2, lqaa026 (2020).
Keilwagen, J., Hartung, F., Paulini, M., Twardziok, S. O. & Grau, J. Combining RNA-seq data and homology-based gene prediction for plants, animals and fungi. BMC Bioinform. 19, 189 (2018).
Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786 (2011).
Krogh, A., Larsson, B., von Heijne, G. & Sonnhammer, E. L. L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305, 567–580 (2001).
Camacho, C. et al. BLAST+: architecture and applications. BMC Bioinform. 10, 421 (2009).
El-Gebali, S. et al. The Pfam protein families database in 2019. Nucleic Acids Res. 47, D427–D432 (2019).
Kiełbasa, S. M., Wan, R., Sato, K., Horton, P. & Frith, M. C. Adaptive seeds tame genomic sequence comparison. Genome Res. 21, 487–493 (2011).
Yang, Y., Li, Y., Chen, Q., Sun, Y. & Lu, Z. WGDdetector: a pipeline for detecting whole genome duplication events using the genome or transcriptome annotations. BMC Bioinform. 20, 75 (2019).
Peterson, B. K., Weber, J. N., Kay, E. H., Fisher, H. S. & Hoekstra, H. E. Double digest RADseq: An inexpensive method for de novo SNP discovery and genotyping in model and non-model species. PLoS ONE 7, e37135 (2012).
Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139–140 (2010).
Bailey, T. L., Johnson, J., Grant, C. E. & Noble, W. S. The MEME Suite. Nucleic Acids Res. 43, W39–W49 (2015).
Kriventseva, E. V. et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 47, D807–D811 (2019).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Zhang, G.-Q. et al. The Apostasia genome and the evolution of orchids. Nature 549, 379–383 (2017).
Suetsugu, K. et al. Transcriptomic heterochrony and completely cleistogamous flower development in the mycoheterotrophic orchid Gastrodia. New Phytol. 237, 323–338 (2023).
Fukushima, K. & Pollock, D. D. Amalgamated cross-species transcriptomes reveal organ-specific propensity in gene expression evolution. Nat. Commun. 11, 4459 (2020).
Huerta-Cepas, J. et al. The human phylome. Genome Biol. 8, 934–941 (2007).
Guéguen, L. & Duret, L. Unbiased estimate of synonymous and nonsynonymous substitution rates with nonstationary base composition. Mol. Biol. Evol. 35, 734–742 (2018).
Fukushima, K. & Pollock, D. D. Detecting macroevolutionary genotype–phenotype associations using error-corrected rates of protein convergence. Nat. Ecol. Evol. 7, 155–170 (2023).
Vollger, M. R., Kerpedjiev, P., Phillippy, A. M. & Eichler, E. E. StainedGlass: interactive visualization of massive tandem repeat structures with identity heatmaps. Bioinformatics 38, 2049–2051 (2022).
Dr. Thomas Hughes is a UK-based scientist and science communicator who makes complex topics accessible to readers. His articles explore breakthroughs in various scientific disciplines, from space exploration to cutting-edge research.