Journal Article

Comparative cell-specific transcriptomics reveals differentiation of C₄ photosynthesis pathways in switchgrass and other C₄ lineages

Li, Guifen, Lu, Nan, Tang, Yuhong, Nakashima, Jin, Rao, Xiaolan, Dixon, Richard A.

2016

Overview

Almost all C₄ plants require the co-ordination of the adjacent and fully differentiated cell types, mesophyll (M) and bundle sheath (BS). The C₄ photosynthetic pathway operates through two distinct subtypes based on how malate is decarboxylated in BS cells; through NAD-malic enzyme (NAD-ME) or NADP-malic enzyme (NADP-ME). The diverse or unique cell-specific molecular features of M and BS cells from separate C₄ subtypes of independent lineages remain to be determined. We here provide an M/BS cell type-specific transcriptome data set from the monocot NAD-ME subtype switchgrass (Panicum virgatum). A comparative transcriptomics approach was then applied to compare the M/BS mRNA profiles of switchgrass, monocot NADP-ME subtype C₄ plants maize and Setaria viridis, and dicot NAD-ME subtype Cleome gynandra. We evaluated the convergence in the transcript abundance of core components in C₄ photosynthesis and transcription factors to establish Kranz anatomy, as well as gene distribution of biological functions, in these four independent C₄ lineages. We also estimated the divergence between NAD-ME and NADP-ME subtypes of C₄ photosynthesis in the two cell types within C₄ species, including differences in genes encoding decarboxylating enzymes, aminotransferases, and metabolite transporters, and differences in the cell-specific functional enrichment of RNA regulation and protein biogenesis/homeostasis. We suggest that C₄ plants of independent lineages in both monocots and dicots underwent convergent evolution to establish C₄ photosynthesis, while distinct C₄ subtypes also underwent divergent processes for the optimization of M and BS cell co-ordination. The comprehensive data sets in our study provide a basis for further research on evolution of C₄ species.

• Publisher: Oxford University Press
• Subject: Biological Transport / Carbon - metabolism / Cell Differentiation / Cell Separation / Chromosome Mapping / Gene Expression Regulation, Plant / High-Throughput Nucleotide Sequencing / In Situ Hybridization / Malate Dehydrogenase - metabolism / Mesophyll Cells - metabolism / Models, Biological / Panicum - cytology / Panicum - genetics / Photosynthesis - genetics / Phylogeny / Plant Leaves - genetics / Plant Proteins - metabolism / Plant Vascular Bundle - genetics / RESEARCH PAPER / RNA, Messenger - genetics / RNA, Messenger - metabolism / Transcription Factors - metabolism / Transcriptome - genetics