Independent Recruitment of Duplicated β-Subunit-Coding NAD-ME Genes Aided the Evolution of C4 Photosynthesis in Cleomaceae.
Independent Recruitment of Duplicated β-Subunit-Coding NAD-ME Genes Aided the Evolution of C4 Photosynthesis in Cleomaceae.
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DOI：
10.3389/fpls.2020.572080
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发表时间：
2020
影响因子：
5.6
通讯作者：
Maurino VG
中科院分区：
文献类型：
--
作者：
Tronconi MA;Hüdig M;Schranz ME;Maurino VG
在C4植物的不同谱系中，通过Rubisco附近的C4酸脱羧释放CO2由NADP-苹果酸酶（ME）或NAD-ME催化，并且兼性使用磷酸烯醇式丙酮酸羧激酶。C4-NADP-ME进化过程中基因谱系的协同选择作用已被深入研究，而C4-NAD-ME进化过程中基因谱系的协同选择作用研究较少。在这项工作中，我们的目的是阐明NAD-ME的招募机制，其功能在C4途径的重点是真双子叶植物科Cleomaceae。我们在维管植物中鉴定了NAD-ME的重复，产生了两种旁系同源物谱系：α-和β-NAD-ME。这两种基因谱系在种子植物中保留，它们的固定可能是由亚功能化的退化过程驱动的，这导致NAD-ME主要作为α-和β-亚基的异聚体运行。我们发现大多数被子植物基因组保持1：1的β-NAD-ME/α-NAD-ME（β/α）相对基因剂量，但也有一些显著的例外，主要是由于β-NAD-ME亚基的额外重复。例如，具有C4-NAD-ME型光合作用的物种的显著高比例具有非1：1的β/α比率。在油菜目中，我们发现C4物种由于β-NAD-ME重复（β1和β2）而具有2：1的比例;这在C3 Tarenaya hassleriana和芸苔属作物中也观察到。在独立进化的C4物种Gynandropsis gynandra和Cleome angustifolia中，所有三个基因都受到C4进化的影响，α-和β1-NAD-ME由适应性选择驱动。特别是β1-NAD-ME与其他物种和同种的β2-NAD-ME相比具有许多差异取代的氨基酸。其中5个氨基酸在G的β1-NAD-ME中被完全取代。gynandra和C. angustifolia，其中两个被鉴定为正选择。通过同线分析，我们确定β-NAD-ME重复来自古老的多倍性事件，α-NAD-ME在Cleomaceae和菊科中都处于独特的同线背景中。我们讨论了我们对NAD-ME的进化及其对C4光合作用的补充的假设。我们建议，基因重复提供了在C4 Cleomaceae的NAD-ME的招聘的基础上，NAD-ME基因家族的所有成员已适应，以适应C4-生物化学。此外，其中一个β-NAD-ME基因拷贝独立地在C4途径中发挥其功能。
In different lineages of C4 plants, the release of CO2 by decarboxylation of a C4 acid near rubisco is catalyzed by NADP-malic enzyme (ME) or NAD-ME, and the facultative use of phosphoenolpyruvate carboxykinase. The co-option of gene lineages during the evolution of C4-NADP-ME has been thoroughly investigated, whereas that of C4-NAD-ME has received less attention. In this work, we aimed at elucidating the mechanism of recruitment of NAD-ME for its function in the C4 pathway by focusing on the eudicot family Cleomaceae. We identified a duplication of NAD-ME in vascular plants that generated the two paralogs lineages: α- and β-NAD-ME. Both gene lineages were retained across seed plants, and their fixation was likely driven by a degenerative process of sub-functionalization, which resulted in a NAD-ME operating primarily as a heteromer of α- and β-subunits. We found most angiosperm genomes maintain a 1:1 β-NAD-ME/α-NAD-ME (β/α) relative gene dosage, but with some notable exceptions mainly due to additional duplications of β-NAD-ME subunits. For example, a significantly high proportion of species with C4-NAD-ME-type photosynthesis have a non-1:1 ratio of β/α. In the Brassicales, we found C4 species with a 2:1 ratio due to a β-NAD-ME duplication (β1 and β2); this was also observed in the C3 Tarenaya hassleriana and Brassica crops. In the independently evolved C4 species, Gynandropsis gynandra and Cleome angustifolia, all three genes were affected by C4 evolution with α- and β1-NAD-ME driven by adaptive selection. In particular, the β1-NAD-MEs possess many differentially substituted amino acids compared with other species and the β2-NAD-MEs of the same species. Five of these amino acids are identically substituted in β1-NAD-ME of G. gynandra and C. angustifolia, two of them were identified as positively selected. Using synteny analysis, we established that β-NAD-ME duplications were derived from ancient polyploidy events and that α-NAD-ME is in a unique syntenic context in both Cleomaceae and Brassicaceae. We discuss our hypotheses for the evolution of NAD-ME and its recruitment for C4 photosynthesis. We propose that gene duplications provided the basis for the recruitment of NAD-ME in C4 Cleomaceae and that all members of the NAD-ME gene family have been adapted to fit the C4-biochemistry. Also, one of the β-NAD-ME gene copies was independently co-opted for its function in the C4 pathway.
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