Abstract

Conservative gene families in plants, which are closely related to innovations in flowering plants, have long and complex evolutionary histories. Here, we used the SQUAMOSA promoter-binding protein (SBP-box) gene family as an example to study conservative gene families in flowering plants. In total, 11 groups, including nine angiosperm-conservative groups and two monocot- and eudicot-specific groups, were identified. Among the nine angiosperm-conservative groups, four are conserved in all land plants and the remaining five are angiosperm-specific. The five angiosperm-specific groups exhibit structural and functional diversity and evolved together, along with the evolution of flowering plants. The expansion of SBP genes was affected by miR156, and the miR156-regulated SBP genes tend to retain more copies. Our results reflect the dynamic evolutionary process of the different groups, with the identification of two genetic lines via synteny analyses. In addition, miR156 showed a close evolutionary relationship with SBP genes, suggesting that it may originate from face-to-face tandem duplication of SBP genes. SBP genes without an miR156 binding locus are usually functionally conservative or housekeeping like, belonging to the terrestrial-conservative group. In contrast, SBP genes with miR156 binding sites are selected by angiosperms to regulate more complex physiological processes.

Highlights

  • Angiosperms, with at least 300,000 species in multiple families, are the most diverse and latest-diverging group in the plant kingdom [1,2,3,4]

  • The genomic and proteomic sequences of Brachypodium distachyon, Ananas comosus, Sorghum bicolor, Panicum hallii, Oryza sativa, Musa acuminate, Setaria italica, Elaeis guineensis, Zea mays, Brassica rapa, Camelina sativa, Phaseolus vulgaris, Vigna angularis, Cajanus cajan, Medicago truncatula, Solanum lycopersicum, Capsicum annuum, Nicotiana tabacum, Prunus persica, Malus domestica, and Prunus mume were taken from the NCBI database [33]

  • The SBP protein sequences for A. thaliana, O. sativa, Physcomitrella patens, Selaginella moellendorffii, Picea abies, Amborella trichopoda, and Chlamydomonas reinhardtii were obtained from the PlantTFDB database [35]

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Summary

Introduction

Angiosperms (flowering plants), with at least 300,000 species in multiple families, are the most diverse and latest-diverging group in the plant kingdom [1,2,3,4]. There are many conservative gene families in flowering plants. They appear in a large range of taxa and often play critical roles. Some gene families are the main catalytic carriers of important biochemical processes in plants. The P450 super family has a large number of plant members and is the key enzyme for chemical synthesis [5,6]; some conservative families are important transcription factors (TFs), which, in plants, are structurally diverse and involved in many development processes and responses to abiotic and biotic stresses. The WRKY superfamily is involved in pathogen defense [7], senescence, and trichome development [8,9], and the MADS-box gene family is strongly correlated with the origin and evolution of reproductive structures such as flowers and ovules [10]

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