title: Disruption of the petal identity gene APETALA3-3 is highly correlated with loss of petals within the buttercup family (Ranunculaceae).
abstract: Absence of petals, or being apetalous, is usually one of the most important features that characterizes a group of flowering plants at high taxonomic ranks (i.e., family and above). The apetalous condition, however, appears to be the result of parallel or convergent evolution with unknown genetic causes. Here we show that within the buttercup family (Ranunculaceae), apetalous genera in at least seven different lineages were all derived from petalous ancestors, indicative of parallel petal losses. We also show that independent petal losses within this family were strongly associated with decreased or eliminated expression of a single floral organ identity gene, APETALA3-3 (AP3-3), apparently owing to species-specific molecular lesions. In an apetalous mutant of Nigella, insertion of a transposable element into the second intron has led to silencing of the gene and transformation of petals into sepals. In several naturally occurring apetalous genera, such as Thalictrum, Beesia, and Enemion, the gene has either been lost altogether or disrupted by deletions in coding or regulatory regions. In Clematis, a large genus in which petalous species evolved secondarily from apetalous ones, the gene exhibits hallmarks of a pseudogene. These results suggest that, as a petal identity gene, AP3-3 has been silenced or down-regulated by different mechanisms in different evolutionary lineages. This also suggests that petal identity did not evolve many times independently across the Ranunculaceae but was lost in numerous instances. The genetic mechanisms underlying the independent petal losses, however, may be complex, with disruption of AP3-3 being either cause or effect.
authors.affiliation: State Key Laboratory of Systematic and Evolutionary Botany, Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China.
authors.forename: Rui
authors.initials: R
authors.lastname: Zhang
authors.forename: Chunce
authors.initials: C
authors.lastname: Guo
authors.forename: Wengen
authors.initials: W
authors.lastname: Zhang
authors.forename: Peipei
authors.initials: P
authors.lastname: Wang
authors.forename: Lin
authors.initials: L
authors.lastname: Li
authors.forename: Xiaoshan
authors.initials: X
authors.lastname: Duan
authors.forename: Qinggao
authors.initials: Q
authors.lastname: Du
authors.forename: Liang
authors.initials: L
authors.lastname: Zhao
authors.forename: Hongyan
authors.initials: H
authors.lastname: Shan
authors.forename: Scott A
authors.initials: SA
authors.lastname: Hodges
authors.forename: Elena M
authors.initials: EM
authors.lastname: Kramer
authors.forename: Yi
authors.initials: Y
authors.lastname: Ren
authors.forename: Hongzhi
authors.initials: H
authors.lastname: Kong
mesh_terms: D004251:DNA Transposable Elements / Q000502:physiology; D019143:Evolution, Molecular; D035264:Flowers / Q000235:genetics / Q000378:metabolism*; D018506:Gene Expression Regulation, Plant / Q000502:physiology*; D020868:Gene Silencing / Q000502:physiology; D026161:MADS Domain Proteins / Q000096:biosynthesis* / Q000235:genetics; D016254:Mutagenesis, Insertional; D010940:Plant Proteins / Q000096:biosynthesis* / Q000235:genetics; D029626:Ranunculaceae / Q000235:genetics / Q000378:metabolism*
chemical_list: D004251:DNA Transposable Elements; D026161:MADS Domain Proteins; D010940:Plant Proteins