Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits

doi:10.1111/jipb.13618

J Integr Plant Biol. ›› 2024, Vol. 66 ›› Issue (2): 228-251.DOI: 10.1111/jipb.13618

• Molecular Ecology and Evolution • Previous Articles Next Articles

Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits

Yezi Xiang^1,2†, Taikui Zhang^1,3†, Yiyong Zhao^1†, Hongjin Dong⁴, Hongyi Chen⁴, Yi Hu³, Chien‐Hsun Huang¹, Jun Xiang^4* and Hong Ma^3*

1. State Key Laboratory of Genetic Engineering, Ministry of Education Key Laboratory of Biodiversity and Ecological Engineering, Institute of Plant Biology, Center of Evolutionary Biology, School of Life Sciences, Fudan University, Shanghai 200438, China;
2. Department of Biology, Howard Hughes Medical Institute, Duke University, Durham, NC 27708, USA;
3. Department of Biology, the Eberly College of Science, and the Huck Institutes of the Life Sciences, the Pennsylvania State University, University Park, PA 16802, USA;
4. Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization, College of Biology and Agricultural Resources, Huanggang Normal University, Huanggang 438000, China
^†These authors contributed equally to this work.
^*Correspondences: Jun Xiang (swxj@hgnu.edu.cn); Hong Ma (hxm16@psu.edu, Dr. Ma is fully responsible for the distributions of all materials associated with this article)

Received:2023-12-15 Accepted:2024-01-11 Online:2024-02-13 Published:2024-02-01

Abstract

Abstract: Fruit functions in seed protection and dispersal and belongs to many dry and fleshy types, yet their evolutionary pattern remains unclear in part due to uncertainties in the phylogenetic relationships among several orders and families. Thus we used nuclear genes of 502 angiosperm species representing 231 families to reconstruct a well supported phylogeny, with resolved relationships for orders and families with previously uncertain placements. Using this phylogeny as a framework, molecular dating supports a Triassic origin of the crown angiosperms, followed by the emergence of most orders in the Jurassic and Cretaceous and their rise to ecological dominance during the Cretaceous Terrestrial Revolution. The robust phylogeny allowed an examination of the evolutionary pattern of fruit and ovary types, revealing a trend of parallel carpel fusions during early diversifications in eudicots, monocots, and magnoliids. Moreover, taxa in the same order or family with the same ovary type can develop either dry or fleshy fruits with strong correlations between specific types of dry and fleshy fruits; such associations of ovary, dry and fleshy fruits define several ovary-fruit “modules” each found in multiple families. One of the frequent modules has an ovary containing multiple ovules, capsules and berries, and another with an ovary having one or two ovules, achenes (or other single-seeded dry fruits) and drupes. This new perspective of relationships among fruit types highlights the closeness of specific dry and fleshy fruit types, such as capsule and berry, that develop from the same ovary type and belong to the same module relative to dry and fleshy fruits of other modules (such as achenes and drupes). Further analyses of gene families containing known genes for ovary and fruit development identified phylogenetic nodes with multiple gene duplications, supporting a possible role of whole-genome duplications, in combination with climate changes and animal behaviors, in angiosperm fruit and ovary diversification.

Key words: angiosperm, fruit evolution, MADS-box, molecular clock, nuclear phylogeny, ovary and fruit developmental genes

Yezi Xiang, Taikui Zhang, Yiyong Zhao, Hongjin Dong, Hongyi Chen, Yi Hu, Chien‐Hsun Huang, Jun Xiang and Hong Ma. Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits[J]. J Integr Plant Biol., 2024, 66(2): 228-251.

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Angiosperm-wide analysis of fruit and ovary evolution aided by a new nuclear phylogeny supports association of the same ovary type with both dry and fleshy fruits

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