Evolutionary diversification of C2 photosynthesis in the grass genus Homolepis (Arthropogoninae)

Joyce Pereira Alvarenga; Matt Stata; Rowan F Sage; Ria Patel; Ane Marcela das Chagas Mendonca; Felipe Della Torre; Hongbing Liu; Shifeng Cheng; Samantha Weake; Emile J Watanabe; Pedro Lage Viana; Iago Augusto de Castro Arruda; Martha Ludwig; João Paulo Rodrigues Alves Delfino Barbosa; Tammy L Sage

doi:10.1093/aob/mcae214

Evolutionary diversification of C2 photosynthesis in the grass genus Homolepis (Arthropogoninae)

Ann Bot. 2024 Dec 17:mcae214. doi: 10.1093/aob/mcae214. Online ahead of print.

Authors

Joyce Pereira Alvarenga^{1

2}, Matt Stata², Rowan F Sage², Ria Patel², Ane Marcela das Chagas Mendonca^{1

2}, Felipe Della Torre^{2

3}, Hongbing Liu⁴, Shifeng Cheng⁴, Samantha Weake², Emile J Watanabe², Pedro Lage Viana⁵, Iago Augusto de Castro Arruda¹, Martha Ludwig⁶, João Paulo Rodrigues Alves Delfino Barbosa¹, Tammy L Sage²

Affiliations

¹ Laboratory of Ecophysiology, Plant Physiology Sector, Department of Biology, Federal University of Lavras, Lavras - MG, Brazil.
² Department of Ecology and Evolutionary Biology, University of Toronto, 25 Willcocks St., Ontario, Canada.
³ Laboratory of Plant Physiology, Department of Botany, Institute of Science Biology, Federal University of Minas Gerais. Belo Horizonte- MG, Brazil.
⁴ Shenzhen Branch, Guangdong Laboratory for Lingnan Modern Agriculture, Genome Analysis Laboratory of the Ministry of Agriculture, Agricultural Genomics Institute at Shenzhen, Chinese Academy of Agricultural Sciences, Shenzhen, 518120, China.
⁵ Instituto Nacional da Mata Atlantica, Santa Teresa, Brazil.
⁶ School of Molecular Sciences, University of Western Australia, Crawley, WA 6009, Australia.

PMID: 39688921
DOI: 10.1093/aob/mcae214

Abstract

Background and aims: To better understand C4 evolution in monocots, we characterized C3-C4 intermediate phenotypes in the grass genus Homolepis (subtribe Arthropogoninae).

Methods: Carbon isotope ratio (δ13C), leaf gas exchange, mesophyll (M) to 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.

Key results: Homolepis contains two C3 (H. glutinosa, H. villaricensis), one 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 GDC 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 ultrastructural, and transcript expression show M. loliiforme is a C4 plant of the NADP-malic enzyme subtype. Homolepis is comprised of two sister clades, one containing H. glutinosa and H. villaricensis and the second H. longispicula and H. aturensis. Homolepis isocalycia is of hybrid origin, with parents being H. aturensis and a common ancestor of the C3 Homolepis clade and H. longispicula.

Conclusions: 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.

Keywords: C2 photosynthesis; C3-C4 intermediate; C4 photosynthesis; carbon concentrating mechanism; glycine decarboxylase; leaf anatomy; photosynthetic evolution.