Anatomical constraints to C-4 evolution:light harvesting capacity in the bundle sheath

Bellasio, Chandra and Lundgren, Marjorie R. (2016) Anatomical constraints to C-4 evolution:light harvesting capacity in the bundle sheath. New Phytologist, 212 (2). pp. 485-496. ISSN 0028-646X

Abstract

In C-4 photosynthesis CO2 assimilation and reduction are typically coordinated across mesophyll (M) and bundle sheath (BS) cells, respectively. This system consequently requires sufficient light to reach BS to generate enough ATP to allow ribulose-1,5-bisphosphate (RuBP) regeneration in BS. Leaf anatomy influences BS light penetration and therefore constrains C-4 cycle functionality. Using an absorption scattering model (coded in Excel, and freely downloadable) we simulate light penetration profiles and rates of ATP production in BS across the C-3, C-3-C-4 and C-4 anatomical continua. We present a trade-off for light absorption between BS pigment concentration and space allocation. C-3 BS anatomy limits light absorption and benefits little from high pigment concentrations. Unpigmented BS extensions increase BS light penetration. C-4 and C-3-C-4 anatomies have the potential to generate sufficient ATP in the BS, whereas typical C-3 anatomy does not, except some C-3 taxa closely related to C-4 groups. Insufficient volume of BS, relative to M, will hamper a C-4 cycle via insufficient BS light absorption. Thus, BS ATP production and RuBP regeneration, coupled with increased BS investments, allow greater operational plasticity. We propose that larger BS in C-3 lineages may be co-opted for C-3-C-4 and C-4 biochemistry requirements.