Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication.

Antagonistic roles for KNOX1 and KNOX2 genes in patterning the land plant body plan following an ancient gene duplication.
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DOI:
10.1371/journal.pgen.1004980
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发表时间:
2015-02
期刊:
影响因子:
4.5
通讯作者:
Bowman JL
Bowman JL
中科院分区:
生物学2区
文献类型:
--
作者:
Furumizu C;Alvarez JP;Sakakibara K;Bowman JL

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基因复制后的新功能化被认为是产生进化新颖性的关键驱动因素之一。陆地植物共同祖先中的基因复制产生了两类 KNOTTED 样 TALE 同源盒基因:I 类 (KNOX1) 和 II 类 (KNOX2)。 KNOX1 基因与开花植物和苔藓孢子体的组织增殖和分生组织潜力的维持有关,KNOX1 活性的调节与开花植物叶形多样性的贡献有关。虽然 KNOX2 功能已被证明可以抑制苔藓孢子体(二倍体)发育过程中的配子体(单倍体)发育程序,但人们对开花植物中的 KNOX2 功能知之甚少,这阻碍了陆地植物进化背景下两类 KNOX 基因之间关系的合成。含有功能丧失的 KNOX2 等位基因的拟南芥植物表现出所有气生器官的分化受损,并且具有高度复杂的叶子,表型与功能获得的 KNOX1 等位基因相似。相反,功能获得性 KNOX2 等位基因与假定的异二聚体 BELL TALE 同源盒伙伴结合抑制了拟南芥中的 SAM 活性,并降低了拟南芥近缘碎米荠中的叶片复杂性,这让人想起功能丧失的 KNOX1 等位基因。几乎没有发现证据表明 KNOX1 和 KNOX2 基因之间存在上位性或相互抑制。 KNOX 蛋白与 BELL TALE 同源框蛋白异二聚化形成功能复合物,与早期基于体外和异源表达的报道相反,我们发现 KNOX 和 BELL 伴侣在体内具有高选择性。因此,KNOX2 基因赋予 KNOX1 基因相反的活性,而不是冗余的作用,并且它们共同指导拟南芥孢子体所有地上器官的发育。我们推断,在陆地植物祖先中 KNOX1/KNOX2 基因复制之后,新功能化导致了拮抗生化活性的进化,从而促进了更复杂的孢子体转录网络的进化,为陆地植物体计划的形态进化提供了可塑性。真核生物在其生命周期中在单倍体(1n)和二倍体(2n)阶段之间交替,并且经常看到它们之间在形态和生理学上的显着差异。陆生植物在两代中都是多细胞的,这与它们假定的祖先绿藻相反,绿藻仅在单倍体阶段发展出多细胞性。 TALE 类同源域转录因子在真核生物不同谱系的二倍体发育激活中发挥着关键作用。该家族中陆地植物祖先的基因复制事件对陆地植物的进化具有深远的影响。我们表明,基因复制事件产生的两个亚类以互补的方式作用于开花植物拟南芥二倍体阶段的大多数地上器官。它们相反的活动塑造了从整个叶子到羽状叶子的形状,并控制植物体的结构,从而为进化修补提供了可塑性。这些结果为理解这些基因如何从调节受精卵中二倍体基因表达的祖先作用转变为指导孢子体陆地植物体结构奠定了基础,并为了解各种形式的生命周期的进化提供了见解。
Neofunctionalization following gene duplication is thought to be one of the key drivers in generating evolutionary novelty. A gene duplication in a common ancestor of land plants produced two classes of KNOTTED-like TALE homeobox genes, class I (KNOX1) and class II (KNOX2). KNOX1 genes are linked to tissue proliferation and maintenance of meristematic potentials of flowering plant and moss sporophytes, and modulation of KNOX1 activity is implicated in contributing to leaf shape diversity of flowering plants. While KNOX2 function has been shown to repress the gametophytic (haploid) developmental program during moss sporophyte (diploid) development, little is known about KNOX2 function in flowering plants, hindering syntheses regarding the relationship between two classes of KNOX genes in the context of land plant evolution. Arabidopsis plants harboring loss-of-function KNOX2 alleles exhibit impaired differentiation of all aerial organs and have highly complex leaves, phenocopying gain-of-function KNOX1 alleles. Conversely, gain-of-function KNOX2 alleles in conjunction with a presumptive heterodimeric BELL TALE homeobox partner suppressed SAM activity in Arabidopsis and reduced leaf complexity in the Arabidopsis relative Cardamine hirsuta, reminiscent of loss-of-function KNOX1 alleles. Little evidence was found indicative of epistasis or mutual repression between KNOX1 and KNOX2 genes. KNOX proteins heterodimerize with BELL TALE homeobox proteins to form functional complexes, and contrary to earlier reports based on in vitro and heterologous expression, we find high selectivity between KNOX and BELL partners in vivo. Thus, KNOX2 genes confer opposing activities rather than redundant roles with KNOX1 genes, and together they act to direct the development of all above-ground organs of the Arabidopsis sporophyte. We infer that following the KNOX1/KNOX2 gene duplication in an ancestor of land plants, neofunctionalization led to evolution of antagonistic biochemical activity thereby facilitating the evolution of more complex sporophyte transcriptional networks, providing plasticity for the morphological evolution of land plant body plans. Eukaryotes alternate between haploid (1n) and diploid (2n) stages during their life cycles, and often seen are remarkable differences in morphology and physiology between them. Land plants are multicellular in both generations, in contrast to their presumed ancestral green algae that develop multicellularity only in the haploid stage. TALE class homeodomain transcriptional factors play a key role in the activation of diploid development in diverse lineages of eukaryotes. A gene duplication event within this family in an ancestor of land plants had profound implications for land plant evolution. We show that the two subclasses resulting from the gene duplication event act to pattern, in a complementary manner, most above ground organs of the diploid stage of the flowering plant Arabidopsis. Their opposing activities sculpt the shape of leaves from entire to pinnate and control the architecture of the plant body, and thus providing plasticity for evolutionary tinkering. These results form a foundation for understanding how these genes have been co-opted from an ancestral role of regulating diploid gene expression in a zygote to directing sporophyte land plant body architecture and provide insight into the evolution of various forms of life cycles.
DOI: 10.1007/bf00021196
发表时间: 1995-07-01
影响因子: 5.1
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