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
中科院分区:
文献类型:
--
作者:
Furumizu C;Alvarez JP;Sakakibara K;Bowman JL
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.
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影响因子:
5.1
作者:
DOCKX, J;QUAEDVLIEG, N;SMEEKENS, S
通讯作者:
SMEEKENS, S
影响因子:
9.2
作者:
Hofer, J;Turner, L;Ellis, N
通讯作者:
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DOI:
10.1073/pnas.0501181102
发表时间:
2005-03-29
影响因子:
11.1
作者:
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通讯作者:
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影响因子:
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作者:
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通讯作者:
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影响因子:
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作者:
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通讯作者:
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