Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología (CNB), Consejo Superior de Investigaciones Científicas (CSIC), Madrid 28049, Spain.
Departamento de Ecología Integrativa, Estación Biológica de Doñana (EBD), Consejo Superior de Investigaciones Científicas (CSIC), Sevilla 41092, Spain.
Plant Cell. 2021 May 5;33(3):548-565. doi: 10.1093/plcell/koaa041.
Both inter- and intra-specific diversity has been described for trichome patterning in fruits, which is presumably involved in plant adaptation. However, the mechanisms underlying this developmental trait have been hardly addressed. Here we examined natural populations of Arabidopsis (Arabidopsis thaliana) that develop trichomes in fruits and pedicels, phenotypes previously not reported in the Arabidopsis genus. Genetic analyses identified five loci, MALAMBRUNO 1-5 (MAU1-5), with MAU2, MAU3, and MAU5 showing strong epistatic interactions that are necessary and sufficient to display these traits. Functional characterization of these three loci revealed cis-regulatory mutations in TRICHOMELESS1 and TRIPTYCHON, as well as a structural mutation in GLABRA1. Therefore, the multiple mechanisms controlled by three MYB transcription factors of the core regulatory network for trichome patterning have jointly been modulated to trigger trichome development in fruits. Furthermore, analyses of worldwide accessions showed that these traits and mutations only occur in a highly differentiated relict lineage from the Iberian Peninsula. In addition, these traits and alleles were associated with low spring precipitation, which suggests that trichome development in fruits and pedicels might be involved in climatic adaptation. Thus, we show that the combination of synergistic mutations in a gene regulatory circuit has driven evolutionary innovations in fruit trichome patterning in Arabidopsis.
果实表皮毛模式在种间和种内都具有多样性，这可能与植物的适应有关。然而，这种发育特征的机制还没有得到充分的研究。在这里，我们研究了拟南芥（Arabidopsis thaliana）的自然种群，这些种群在果实和花梗上发育表皮毛，这是以前在拟南芥属中没有报道过的表型。遗传分析确定了五个位点，MALAMBRUNO 1-5（MAU1-5），其中 MAU2、MAU3 和 MAU5 表现出强烈的上位性相互作用，这是表现这些特征所必需和充分的。对这三个位点的功能特征进行了研究，发现 TRICHOMELESS1 和 TRIPTYCHON 中存在顺式调控突变，以及 GLABRA1 中的结构突变。因此，由三个 MYB 转录因子组成的核心调控网络控制的多种机制被共同调节，以触发果实表皮毛的发育。此外，对全球采集品系的分析表明，这些特征和突变仅发生在伊比利亚半岛的一个高度分化的残余谱系中。此外，这些特征和等位基因与春季降水低有关，这表明果实和花梗表皮毛的发育可能与气候适应有关。因此，我们表明，协同突变在基因调控回路中的组合驱动了拟南芥果实表皮毛模式的进化创新。
