Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of C4 photosynthesis.

Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of C4 photosynthesis.
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DOI:
10.1371/journal.pgen.1004365
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发表时间:
2014-06
期刊:
影响因子:
4.5
通讯作者:
Hibberd JM
Hibberd JM
中科院分区:
生物学2区
文献类型:
--
作者:
Aubry S;Kelly S;Kümpers BM;Smith-Unna RD;Hibberd JM

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至少有60个独立的起源跨越单子叶植物和双子叶植物,C4光合作用途径是收敛进化的最杰出的例子之一。 C4光合作用是未知的。这些物种。光合作用的成熟物可能是由单子叶的最后一个共同的祖先和双子叶植物衍生而来的。曾经此外,请确定调节器。 C4光合作用是收敛进化的最成功和宽度的例子之一;但是,从C3到C4的过渡涉及叶片解剖学和生物化学,尽管这些变化多种多样,C4光合作用至少是通过DNA和RNA测序的60次。开发一个新的信息框架,以表明C4植物的两个独立谱系与基因表达的相同调节剂产生了C4叶子,我们的发现提供了一个新的范式,用于研究收敛性状的基因和收敛性表型的起源。
With at least 60 independent origins spanning monocotyledons and dicotyledons, the C4 photosynthetic pathway represents one of the most remarkable examples of convergent evolution. The recurrent evolution of this highly complex trait involving alterations to leaf anatomy, cell biology and biochemistry allows an increase in productivity by ∼50% in tropical and subtropical areas. The extent to which separate lineages of C4 plants use the same genetic networks to maintain C4 photosynthesis is unknown. We developed a new informatics framework to enable deep evolutionary comparison of gene expression in species lacking reference genomes. We exploited this to compare gene expression in species representing two independent C4 lineages (Cleome gynandra and Zea mays) whose last common ancestor diverged ∼140 million years ago. We define a cohort of 3,335 genes that represent conserved components of leaf and photosynthetic development in these species. Furthermore, we show that genes encoding proteins of the C4 cycle are recruited into networks defined by photosynthesis-related genes. Despite the wide evolutionary separation and independent origins of the C4 phenotype, we report that these species use homologous transcription factors to both induce C4 photosynthesis and to maintain the cell specific gene expression required for the pathway to operate. We define a core molecular signature associated with leaf and photosynthetic maturation that is likely shared by angiosperm species derived from the last common ancestor of the monocotyledons and dicotyledons. We show that deep evolutionary comparisons of gene expression can reveal novel insight into the molecular convergence of highly complex phenotypes and that parallel evolution of trans-factors underpins the repeated appearance of C4 photosynthesis. Thus, exploitation of extant natural variation associated with complex traits can be used to identify regulators. Moreover, the transcription factors that are shared by independent C4 lineages are key targets for engineering the C4 pathway into C3 crops such as rice. C4 photosynthesis is one of the most successful and widespread examples of convergent evolution; the first C4 plant evolved long after the extinction of the dinosaurs, yet C4 species now account for ∼30% of primary productivity on earth. Compared with ancestral C3 photosynthesis, the C4 pathway allows faster rates of growth, and thus international efforts have been mustered to introduce advantageous C4 traits into important C3 crops to increase their yield. However, the transition from C3 to C4 involves complex alterations to leaf anatomy and biochemistry. Despite these multiple changes, C4 photosynthesis has evolved independently at least 60 times. Through DNA and RNA sequencing we are beginning define a catalog of genes associated with C3 or C4 photosynthesis. However, we know little about how these genes act co-ordinately to bring about the convergent C4 phenotype. In this work we develop a new informatics framework to reveal that two independent lineages of C4 plants have co-opted the same regulators of gene expression to generate the C4 leaf. Our findings provide a new paradigm for investigating the genetics of convergent traits and the origin of convergent phenotypes. Moreover, they reveal significant new insight into the regulatory mechanisms governing the origins of C4 photosynthesis.
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