title: Comparative cell-specific transcriptomics reveals differentiation of C4 photosynthesis pathways in switchgrass and other C4 lineages.
abstract: 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.
authors.affiliation: Department of Biological Sciences, University of North Texas, 1155 Union Circle #305220, Denton, TX 76203, USA BioEnergy Science Center (BESC), US Department of Energy, Oak Ridge, TN 37831, USA.
authors.forename: Xiaolan
authors.initials: X
authors.lastname: Rao
authors.affiliation: Department of Biological Sciences, University of North Texas, 1155 Union Circle #305220, Denton, TX 76203, USA.
authors.forename: Nan
authors.initials: N
authors.lastname: Lu
authors.affiliation: Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA.
authors.forename: Guifen
authors.initials: G
authors.lastname: Li
authors.affiliation: Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA.
authors.forename: Jin
authors.initials: J
authors.lastname: Nakashima
authors.affiliation: BioEnergy Science Center (BESC), US Department of Energy, Oak Ridge, TN 37831, USA Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA.
authors.forename: Yuhong
authors.initials: Y
authors.lastname: Tang
authors.affiliation: Department of Biological Sciences, University of North Texas, 1155 Union Circle #305220, Denton, TX 76203, USA BioEnergy Science Center (BESC), US Department of Energy, Oak Ridge, TN 37831, USA richard.dixon@unt.edu.
authors.forename: Richard A
authors.initials: RA
authors.lastname: Dixon
mesh_terms: D001692:Biological Transport; D002244:Carbon / Q000378:metabolism; D002454:Cell Differentiation; D002469:Cell Separation; D002874:Chromosome Mapping; D018506:Gene Expression Regulation, Plant; D059014:High-Throughput Nucleotide Sequencing; D017403:In Situ Hybridization; D008291:Malate Dehydrogenase / Q000378:metabolism; D058503:Mesophyll Cells / Q000378:metabolism; D008954:Models, Biological; D008897:Panicum / Q000166:cytology* / Q000235:genetics*; D010788:Photosynthesis / Q000235:genetics*; D010802:Phylogeny; D018515:Plant Leaves / Q000235:genetics; D010940:Plant Proteins / Q000378:metabolism; D058526:Plant Vascular Bundle / Q000235:genetics; D012333:RNA, Messenger / Q000235:genetics / Q000378:metabolism; D014157:Transcription Factors / Q000378:metabolism; D059467:Transcriptome / Q000235:genetics*
chemical_list: D010940:Plant Proteins; D012333:RNA, Messenger; D014157:Transcription Factors; D002244:Carbon; D008291:Malate Dehydrogenase; C046446:malate dehydrogenase-(oxaloacetate-decarboxylating) (NAD+); C031917:malate dehydrogenase (oxaloacetate-decarboxylating) (NADP+)
keywords: C4 photosynthesis; carbon fixation; cell-specific transcriptomics; comparative transcriptomics; switchgrass.