John Christopher R, Smith-Unna Richard D, Woodfield Helen, Covshoff Sarah, Hibberd Julian M
Department of Plant Sciences, University of Cambridge, Cambridge CB2 3EA, United Kingdom.
Plant Physiol. 2014 May;165(1):62-75. doi: 10.1104/pp.114.238667. Epub 2014 Mar 27.
Leaves of almost all C4 lineages separate the reactions of photosynthesis into the mesophyll (M) and bundle sheath (BS). The extent to which messenger RNA profiles of M and BS cells from independent C4 lineages resemble each other is not known. To address this, we conducted deep sequencing of RNA isolated from the M and BS of Setaria viridis and compared these data with publicly available information from maize (Zea mays). This revealed a high correlation (r=0.89) between the relative abundance of transcripts encoding proteins of the core C4 pathway in M and BS cells in these species, indicating significant convergence in transcript accumulation in these evolutionarily independent C4 lineages. We also found that the vast majority of genes encoding proteins of the C4 cycle in S. viridis are syntenic to homologs used by maize. In both lineages, 122 and 212 homologous transcription factors were preferentially expressed in the M and BS, respectively. Sixteen shared regulators of chloroplast biogenesis were identified, 14 of which were syntenic homologs in maize and S. viridis. In sorghum (Sorghum bicolor), a third C4 grass, we found that 82% of these trans-factors were also differentially expressed in either M or BS cells. Taken together, these data provide, to our knowledge, the first quantification of convergence in transcript abundance in the M and BS cells from independent lineages of C4 grasses. Furthermore, the repeated recruitment of syntenic homologs from large gene families strongly implies that parallel evolution of both structural genes and trans-factors underpins the polyphyletic evolution of this highly complex trait in the monocotyledons.
几乎所有C4植物谱系的叶片都将光合作用反应分隔在叶肉细胞（M）和维管束鞘细胞（BS）中。来自独立C4植物谱系的叶肉细胞和维管束鞘细胞的信使RNA谱彼此相似的程度尚不清楚。为了解决这个问题，我们对绿色狗尾草叶肉细胞和维管束鞘细胞分离出的RNA进行了深度测序，并将这些数据与来自玉米（Zea mays）的公开信息进行比较。这揭示了这些物种中叶肉细胞和维管束鞘细胞中编码核心C4途径蛋白的转录本相对丰度之间存在高度相关性（r = 0.89），表明在这些进化上独立的C4植物谱系中，转录本积累存在显著趋同。我们还发现，绿色狗尾草中绝大多数编码C4循环蛋白的基因与玉米使用的同源基因是同线的。在这两个谱系中，分别有122个和212个同源转录因子优先在叶肉细胞和维管束鞘细胞中表达。鉴定出16个叶绿体生物发生的共享调节因子，其中14个是玉米和绿色狗尾草中的同线同源物。在第三种C4禾本科植物高粱（Sorghum bicolor）中，我们发现这些反式作用因子中有82%在叶肉细胞或维管束鞘细胞中也有差异表达。据我们所知，这些数据首次对来自独立C4禾本科植物谱系的叶肉细胞和维管束鞘细胞中转录本丰度的趋同进行了量化。此外，从大型基因家族中反复招募同线同源物强烈表明，结构基因和反式作用因子的平行进化是单子叶植物中这种高度复杂性状多系进化的基础。
