TY - JOUR

T1 - Deconstructing Kranz anatomy to understand C-4 evolution

AU - Lundgren, Marjorie R.

AU - Osborne, Colin P.

AU - Christin, Pascal-Antoine

PY - 2014/7

Y1 - 2014/7

N2 - C-4 photosynthesis is a complex physiological adaptation that confers greater productivity than the ancestral C-3 photosynthetic type in environments where photorespiration is high. It evolved in multiple lineages through the coordination of anatomical and biochemical components, which concentrate CO2 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). In most C-4 plants, the CO2-concentrating mechanism is achieved via the confinement of Rubisco to bundle-sheath cells, into which CO2 is biochemically pumped from surrounding mesophyll cells. The C-4 biochemical pathway relies on a specific suite of leaf functional properties, often referred to as Kranz anatomy. These include the existence of discrete compartments differentially connected to the atmosphere, a close contact between these compartments, and a relatively large compartment to host the Calvin cycle. In this review, we use a quantitative dataset for grasses (Poaceae) and examples from other groups to isolate the changes in anatomical characteristics that generate these functional properties, including changes in the size, number, and distribution of different cell types. These underlying anatomical characteristics vary among C-4 origins, as similar functions emerged via different modifications of anatomical characteristics. In addition, the quantitative characteristics of leaves all vary continuously across C-3 and C-4 taxa, resulting in C-4-like values in some C-3 taxa. These observations suggest that the evolution of C-4-suitable anatomy might require relatively few changes in plant lineages with anatomical predispositions. Furthermore, the distribution of anatomical traits across C-3 and C-4 taxa has important implications for the functional diversity observed among C-4 lineages and for the approaches used to identify genetic determinants of C-4 anatomy.

AB - C-4 photosynthesis is a complex physiological adaptation that confers greater productivity than the ancestral C-3 photosynthetic type in environments where photorespiration is high. It evolved in multiple lineages through the coordination of anatomical and biochemical components, which concentrate CO2 at the active site of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco). In most C-4 plants, the CO2-concentrating mechanism is achieved via the confinement of Rubisco to bundle-sheath cells, into which CO2 is biochemically pumped from surrounding mesophyll cells. The C-4 biochemical pathway relies on a specific suite of leaf functional properties, often referred to as Kranz anatomy. These include the existence of discrete compartments differentially connected to the atmosphere, a close contact between these compartments, and a relatively large compartment to host the Calvin cycle. In this review, we use a quantitative dataset for grasses (Poaceae) and examples from other groups to isolate the changes in anatomical characteristics that generate these functional properties, including changes in the size, number, and distribution of different cell types. These underlying anatomical characteristics vary among C-4 origins, as similar functions emerged via different modifications of anatomical characteristics. In addition, the quantitative characteristics of leaves all vary continuously across C-3 and C-4 taxa, resulting in C-4-like values in some C-3 taxa. These observations suggest that the evolution of C-4-suitable anatomy might require relatively few changes in plant lineages with anatomical predispositions. Furthermore, the distribution of anatomical traits across C-3 and C-4 taxa has important implications for the functional diversity observed among C-4 lineages and for the approaches used to identify genetic determinants of C-4 anatomy.

KW - C-4 photosynthesis

KW - complex trait

KW - convergent evolution

KW - co-option

KW - Kranz anatomy

KW - leaf

KW - BUNDLE-SHEATH-CELLS

KW - PHOTOSYNTHETIC CARBON METABOLISM

KW - FLAVERIA-BROWNII C4-LIKE

KW - LEAF ANATOMY

KW - GRASSES POACEAE

KW - GENOME SIZE

KW - C4 PLANTS

KW - PHENOTYPIC PLASTICITY

KW - VENATION ARCHITECTURE

KW - DIOXIDE COMPENSATION

U2 - 10.1093/jxb/eru186

DO - 10.1093/jxb/eru186

M3 - Review article

VL - 65

SP - 3357

EP - 3369

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

SN - 0022-0957

IS - 13

ER -