Getting the most out of natural variation in C4 photosynthesis

Abstract

C4 photosynthesis is a complex trait that has a high degree of natural variation, involving anatomical and biochemical changes relative to the ancestral C3 state. It has evolved at least 66 times across a variety of lineages and the evolutionary route from C3 to C4 is likely conserved but not necessarily genetically identical. As such, a variety of C4 species are needed to identify what is fundamental to the C4 evolutionary process in a global context. In order to identify the genetic components of C4 form and function, a number of species are used as genetic models. These include Zea mays (maize), Sorghum bicolor (sorghum), Setaria viridis (Setaria), Flaveria bidentis, and Cleome gynandra. Each of these species has different benefits and challenges associated with its use as a model organism. Here, we propose that RNA profiling of a large sampling of C4, C3-C4, and C3 species, from as many lineages as possible, will allow identification of candidate genes necessary and sufficient to confer C4 anatomy and/or biochemistry. Furthermore, C4 model species will play a critical role in the functional characterization of these candidate genes and identification of their regulatory elements, by providing a platform for transformation and through the use of gene expression profiles in mesophyll and bundle sheath cells and along the leaf developmental gradient. Efforts should be made to sequence the genomes of F. bidentis and C. gynandra and to develop congeneric C3 species as genetic models for comparative studies. In combination, such resources would facilitate discovery of common and unique C4 regulatory mechanisms across genera.

Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy

“…Genes controlling development of M and BS specialization for function of the C 4 system, and the degree of redundancy which has occurred during the multiple times C 4 has evolved is unknown. Among monocot and eudicot C 4 species which are being used as genetic models, concerted efforts are needed to identify regulatory factors along leaf developmental gradients which control the expression of specific C 4 traits (Covshoff et al , 2013). …”

“…This includes extensive analysis of leaf development in Zea mays which has classical NADP-ME-type anatomy (Sheen and Bogorad, 1985; Langdale et al , 1988b; Dengler and Nelson, 1999; Sheen, 1999). In the interest of identifying transcription factors controlling expression of specific traits which are required for C 4 function, there have been recent studies on the developmental gradient along the leaf of maize, including analyses of transcriptome, proteome, and structural changes (see Li et al , 2010; Majeran et al , 2010; Covshoff et al , 2013; Wang et al , 2013). Developmental studies have also been conducted on some other forms of Kranz anatomy in grasses (Dengler et al , 1985, 1986, 1996; Wakayama et al , 2003) and on different structural forms of Kranz in family Cyperaceae (Soros and Dengler, 2001).…”

“…Cleome gynandra was originally proposed as a model NAD-ME eudicot C 4 species for identifying factors controlling development and function of C 4 photosynthesis (Brown et al , 2005). The attractive features of this species are that it can be transformed, grown under a short life cycle, has C 3 and C 3 –C 4 intermediate Cleome relatives for comparative studies, and, phylogenetically, among C 4 genera it has the closest position to the well-established model species Arabidopsis thaliana (a C 3 dicot) (Feodorova et al , 2010; Covshoff et al , 2013). Progress towards development of C. gynandra has been made, including identifying transcripts associated with C 4 biochemistry and metabolite transporters (Kajala et al , 2012), in comparative RNaseq profiling (Bräutigam et al , 2011), and in the ability to transform it (Newell et al , 2010).…”

Comparative studies of C3 and C4Atriplex hybrids in the genomics era: physiological assessments

“…Unfortunately, in the case of the C 4 pathway, ideal model organisms have not been developed, although Setaria viridis is a potential candidate (Li and Brutnell, 2011; Covshoff et al , 2014). The lack of tractable genetic models for C 4 photosynthesis requires that alternative means of gene discovery be considered.…”

Photosynthesis and the environment

“…Following this, a set of manuscripts addresses integration of photosynthesis with other key processes including water use and respiration; specifically discussing genetic variation in water use efficiency (Easlon et al 2013), the role of redox state on stomatal regulation (Busch 2013), and the interaction of mitochondrial metabolism and photosynthesis (Araújo et al 2013). The special features of C 4 photosynthesis are then discussed both in terms of natural variation in C 4 Kranz (Covshoff et al 2013), and single-cell C 4 photosynthesis (Sharpe and Offermann 2013). Ultimately, at the molecular and biochemical level, manuscripts address circadian regulation of photosynthesis (Dodd et al 2013), Rubisco (Cavanagh and Kubien 2013), Rubisco activase (Mueller-Cajar et al 2013), pigment regulation of light harvesting (Holleboom and Walla 2013), pigment biosynthesis (Sobotka 2013), thylakoid reactions (Johnson and Ruban 2013) and thylakoid organization (Sznee et al 2013).…”