Kanaris Michael, Lee Jonathan, Chang Belinda, Christendat Dinesh
Department of Cell and Systems Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Department of Ecology and Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
Mol Biol Evol. 2025 Jun 4;42(6). doi: 10.1093/molbev/msaf129.
Shikimate kinase-like 1 (SKL1) plays an essential role in chloroplast biogenesis in Arabidopsis thaliana whereby mutants present a pigment-defective phenotype. The inability to identify SKL1 in organisms predating land plants suggests an important role for this gene coinciding with the emergence of terrestrial plants. A role for SKL1 in chloroplast biogenesis has previously been determined in Arabidopsis; however, the biological function for SKL1 has not been established in early land plants. In the present study, we provided functional and evolutionary insights into the diversification of SKL1 in the early land plant Marchantia polymorpha. We identified the SK gene homologs common to all land plants, two of which were shown to have high sequence similarity to SK. We confirmed that one member possessed shikimate kinase activity, whereas the second member is inactive. These findings led us to identify MpSK (Mp3g21830) and infer the identity of MpSKL1 (Mp6g03600). Consistent with previous studies in Arabidopsis, disruption of MpSKL1 in Marchantia resulted in a pigment-defective phenotype with abnormal chloroplast morphology and thylakoid network organization. Given an early origin of SKL1 in land plant evolution, we investigated requisite structural modifications to an ancestral SK that led to the functional diversification of SKL1. We provided evidence that SKL1 displays an open and accessible substrate binding pocket, conferring its biological function for chloroplast biogenesis. Together, our results demonstrate that the acquisition of SKL1 corresponds with the emergence of terrestrial land plants and that this biological function is conserved across distant plant lineages.
莽草酸激酶样蛋白1（SKL1）在拟南芥叶绿体生物发生中起着至关重要的作用，其突变体呈现色素缺陷型表型。在陆地植物出现之前的生物中无法鉴定出SKL1，这表明该基因在陆地植物出现时发挥了重要作用。此前已在拟南芥中确定了SKL1在叶绿体生物发生中的作用；然而，SKL1在早期陆地植物中的生物学功能尚未明确。在本研究中，我们对早期陆地植物多歧苏铁中SKL1的多样化提供了功能和进化方面的见解。我们鉴定了所有陆地植物共有的SK基因同源物，其中两个与SK具有高度序列相似性。我们证实其中一个成员具有莽草酸激酶活性，而另一个成员无活性。这些发现使我们鉴定出了MpSK（Mp3g21830）并推断出MpSKL1（Mp6g03600）的身份。与之前在拟南芥中的研究一致，多歧苏铁中MpSKL1的破坏导致了色素缺陷型表型，叶绿体形态和类囊体网络组织异常。鉴于SKL1在陆地植物进化中的早期起源，我们研究了对祖先SK进行必要的结构修饰，这些修饰导致了SKL1的功能多样化。我们提供的证据表明，SKL1具有一个开放且可接近的底物结合口袋，赋予其叶绿体生物发生的生物学功能。总之，我们的结果表明SKL1的获得与陆地植物的出现相对应，并且这种生物学功能在遥远的植物谱系中是保守的。
