TY - JOUR

T1 - Anatomical constraints to C-4 evolution

T2 - light harvesting capacity in the bundle sheath

AU - Bellasio, Chandra

AU - Lundgren, Marjorie R.

PY - 2016/10

Y1 - 2016/10

N2 - 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.

AB - 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.

KW - bioengineering

KW - bundle sheath extension

KW - C-3-C-4

KW - crops

KW - grasses

KW - light penetration

KW - light profiles

KW - Poaceae

KW - CYCLIC ELECTRON FLOW

KW - C4 PHOTOSYNTHESIS

KW - LEAF ANATOMY

KW - MAIZE LEAVES

KW - GRASSES POACEAE

KW - PHOTOSYSTEM-I

KW - ZEA-MAYS

KW - MESOPHYLL

KW - PLANTS

KW - DIFFERENTIATION

U2 - 10.1111/nph.14063

DO - 10.1111/nph.14063

M3 - Journal article

VL - 212

SP - 485

EP - 496

JO - New Phytologist

JF - New Phytologist

SN - 0028-646X

IS - 2

ER -