Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, USA.
Department of Biology, University of Central Florida, Orlando, Florida, USA.
Plant Physiol. 2022 Jun 1;189(2):735-753. doi: 10.1093/plphys/kiac116.
C4 photosynthesis and Crassulacean acid metabolism (CAM) have been considered as largely independent adaptations despite sharing key biochemical modules. Portulaca is a geographically widespread clade of over 100 annual and perennial angiosperm species that primarily use C4 but facultatively exhibit CAM when drought stressed, a photosynthetic system known as C4 + CAM. It has been hypothesized that C4 + CAM is rare because of pleiotropic constraints, but these have not been deeply explored. We generated a chromosome-level genome assembly of Portulaca amilis and sampled mRNA from P. amilis and Portulaca oleracea during CAM induction. Gene co-expression network analyses identified C4 and CAM gene modules shared and unique to both Portulaca species. A conserved CAM module linked phosphoenolpyruvate carboxylase to starch turnover during the day-night transition and was enriched in circadian clock regulatory motifs in the P. amilis genome. Preservation of this co-expression module regardless of water status suggests that Portulaca constitutively operate a weak CAM cycle that is transcriptionally and posttranscriptionally upregulated during drought. C4 and CAM mostly used mutually exclusive genes for primary carbon fixation, and it is likely that nocturnal CAM malate stores are shuttled into diurnal C4 decarboxylation pathways, but we found evidence that metabolite cycling may occur at low levels. C4 likely evolved in Portulaca through co-option of redundant genes and integration of the diurnal portion of CAM. Thus, the ancestral CAM system did not strongly constrain C4 evolution because photosynthetic gene networks are not co-regulated for both daytime and nighttime functions.
C4 光合作用和景天酸代谢（CAM）被认为是两种独立的适应策略，尽管它们共享关键的生化模块。马齿苋属是一个广泛分布的类群，包含超过 100 种一年生和多年生被子植物物种，这些物种主要使用 C4 途径，但在干旱胁迫下会兼性地表现出 CAM 途径，这种光合作用系统被称为 C4+CAM。有人假设 C4+CAM 很少见是因为多效性限制，但这些限制并没有被深入研究。我们生成了马齿苋属植物马齿苋的染色体水平基因组组装，并在 CAM 诱导过程中从马齿苋属植物马齿苋和马齿苋中采样 mRNA。基因共表达网络分析鉴定了 C4 和 CAM 基因模块，这些模块在这两个马齿苋属物种中是共享的和独特的。一个保守的 CAM 模块将磷酸烯醇式丙酮酸羧激酶与白天到黑夜的转变过程中的淀粉周转联系起来，并且在马齿苋属植物的基因组中富含生物钟调节基序。无论水势如何，这个共表达模块都能被保存下来，这表明马齿苋属植物持续地运作一个弱的 CAM 循环，在干旱期间，这个循环在转录和转录后被上调。C4 和 CAM 主要使用相互排斥的基因来进行初级碳固定，而且很可能是夜间 CAM 苹果酸库被转移到白天的 C4 脱羧途径中，但我们发现证据表明代谢物循环可能在低水平发生。C4 可能是通过冗余基因的共适应和 CAM 日间部分的整合而在马齿苋属植物中进化而来的。因此，由于光合作用基因网络不是同时受到调控来满足白天和夜间的功能，因此祖先的 CAM 系统并没有强烈限制 C4 的进化。
