Alvarenga Joyce Pereira, Stata Matt, Sage Rowan F, Patel Ria, das Chagas Mendonca Ane Marcela, Della Torre Felipe, Liu Hongbing, Cheng Shifeng, Weake Samantha, Watanabe Emile J, Lage Viana Pedro, de Castro Arruda Iago Augusto, Ludwig Martha, Delfino Barbosa João Paulo Rodrigues Alves, Sage Tammy L
Laboratory of Ecophysiology, Plant Physiology Sector, Department of Biology, Federal University of Lavras, Lavras, Minas Gerais, 37200-900, Brazil.
Department of Ecology and Evolutionary Biology, University of Toronto, Ontario, M5S 3B2, Canada.
Ann Bot. 2025 Mar 13;135(4):769-788. doi: 10.1093/aob/mcae214.
To better understand C4 evolution in monocots, we characterized C3-C4 intermediate phenotypes in the grass genus Homolepis (subtribe Arthropogoninae).
Carbon isotope ratio (δ13C), leaf gas exchange, mesophyll (M) and bundle sheath (BS) tissue characteristics, organelle size and numbers in M and BS tissue, and tissue distribution of the P-subunit of glycine decarboxylase (GLDP) were determined for five Homolepis species and the C4 grass Mesosetum loliiforme from a phylogenetic sister clade. We generated a transcriptome-based phylogeny for Homolepis and Mesosetum species to interpret physiological and anatomical patterns in an evolutionary context, and to test for hybridization.
Homolepis contains two C3 species (H. glutinosa, H. villaricensis), one species with a weaker form of C2 termed sub-C2 (H. isocalycia), and two C2 species (H. longispicula, H. aturensis). Homolepis longispicula and H. aturensis express over 85 % of leaf glycine in centripetal mitochondria within the BS, and have increased fractions of leaf chloroplasts, mitochondria and peroxisomes within the BS relative to H. glutinosa. Analysis of leaf gas exchange, cell ultrastructure and transcript expression show M. loliiforme is a C4 plant of the NADP-malic enzyme subtype. Homolepis comprises two sister clades, one containing H. glutinosa and H. villaricensis and the second H. longispicula and H. aturensis. Homolepis isocalycia is of hybrid origin, its parents being H. aturensis and a common ancestor of the C3 Homolepis clade and H. longispicula.
Photosynthetic activation of BS tissue in the sub-C2 and C2 species of Homolepis is similar to patterns observed in C3-C4 intermediate eudicots, indicating common evolutionary pathways from C3 to C4 photosynthesis in these disparate clades. Hybridization can diversify the C3-C4 intermediate character state and should be considered in reconstructing putative ancestral states using phylogenetic analyses.
为了更好地理解单子叶植物中C4的进化过程，我们对禾本科类芦属（节芒亚族）中C3 - C4中间表型进行了特征分析。
测定了五个类芦属物种以及系统发育姊妹分支中的C4禾本科植物丝状类稷的碳同位素比率（δ13C）、叶片气体交换、叶肉（M）和维管束鞘（BS）组织特征、M和BS组织中细胞器的大小和数量，以及甘氨酸脱羧酶（GLDP）P亚基的组织分布。我们构建了基于转录组的类芦属和类稷属物种系统发育树，以在进化背景下解释生理和解剖模式，并检测杂交情况。
类芦属包含两个C3物种（粘类芦、毛类芦），一个具有较弱形式C2（称为亚C2）的物种（等萼类芦），以及两个C2物种（长穗类芦、阿图类芦）。长穗类芦和阿图类芦在维管束鞘内向心线粒体中表达超过85%的叶片甘氨酸，并且相对于粘类芦，其维管束鞘内叶片叶绿体、线粒体和过氧化物酶体的比例增加。叶片气体交换、细胞超微结构和转录表达分析表明，丝状类稷是NADP - 苹果酸酶亚型的C4植物。类芦属包括两个姊妹分支，一个包含粘类芦和毛类芦，另一个包含长穗类芦和阿图类芦。等萼类芦是杂交起源的，其亲本是阿图类芦以及C3类芦分支和长穗类芦的一个共同祖先。
类芦属亚C2和C2物种中维管束鞘组织的光合激活与在C3 - C4中间真双子叶植物中观察到的模式相似，表明在这些不同分支中从C3到C4光合作用存在共同的进化途径。杂交可以使C3 - C4中间性状状态多样化，在使用系统发育分析重建假定祖先状态时应予以考虑。
