Watching C4 photosynthesis evolve! Does Salsola divaricata, a C2 species on the Canary Islands, bridge the complex evolutionary transition between C3 and C4 photosynthesis?

• Applicant: Professorin Dr. Gudrun Kadereit
• Subject Area: Evolution and Systematics of Plants and Fungi
• Term: from 2015 to 2019
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 282807155

C4 photosynthesis (PS) is a complex trait and its evolution requires profound changes of leaf anatomy and ultrastructure, pathway biochemistry and gene regulation within the ancestral C3 lineage. C4 PS arose c. 65 times in the angiosperms with one hotspot of c. 15 origins in the Chenopodiaceae. The processes of how C4 PS evolved are still a mystery. Conceptual models of C4 evolution always favoured a gradual, stepwise transition from C3 to C4 with the glycine shuttle carbon concentrating mechanisms (C2 PS) as the key step (originally proposed by Monson et al. (1984); modified by Sage et al. 2012). The empirical evidence that supports the model has a number of limitations, most importantly the flaw that phenotypic plasticity and variation of traits at the population level has never been taken into account. To test the current model of C4 evolution this grant proposal suggests to study the C2 species Salsola divaricata from the Canary Islands and the two closely related C3 species S. verticillata and S. gymnomaschala from SW Morocco in which hypothetical early phases of C4 photosynthesis evolution appear to be present. The study includes an assessment of the genetic differentiation among 16 populations of Salsola divaricata and its closest relatives from SW Morocco using the next generation sequencing method genotyping by sequencing, local climate and edaphic parameters and a survey of C4-relevant traits as proposed by the model. These are quantitative assays of C2 and C4 proteins, carbon compensation point measurements, expression patterns of C2 and C4 enzymes in leaf cross sections and bundle sheath ultrastructure. A transcriptome analysis of selected samples with deviating trait expression will furthermore reveal differentiation and/or plasticity at the gene regulatory level. The phenotypic variation of C4 traits in Salsola divaricata might represent distinct genetically fixed evolutionary states of C4 evolution and therefore support the current model or it might be a fascinating case of broad phenotypic plasticity of a complex physiological syndrome and stimulate a fundamental re-evaluation of the current model towards a concept that includes phenotypic plasticity. To understand the evolution of the highly complex trait C4 PS is not only to disentangle a fascinating biological problem of broad interest but also a hot topic in current research efforts to introduce the C4 pathway into C3 crops such as rice.

• DFG Programme: Research Grants