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Significance of C4 Leaf Structure at the Tissue and Cellular Levels

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The Leaf: A Platform for Performing Photosynthesis

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 44))

Summary

The CO2 concentrating mechanism (CCM) in C4 plants requires a complex coordination of both leaf anatomical and biochemical traits. While there are key traits common across the 60 plus C4 lineages, there is also significant structural and biochemical variation. Traditionally, C4 plants are described as one of three biochemical subtypes based on the primary enzyme used for C4 acid decarboxylation: NADP-malic enzyme (NADP-ME), NAD-malic enzyme (NAD-ME), and phosphoenolpyruvate carboxykinase (PCK). However, there may be biochemical flexibility and overlap between these subtypes. C4 plants typically rely on Kranz-type anatomy that partitions the C4 cycle into the mesophyll (M) cells and the majority of C3 cycle into the bundle-sheath (BS) cells. However, within the succulent Chenopods some NAD-ME type C4 plants use one of two single-cell arrangements to partition and compartmentalize the C4 and C3 cycles. Here we discuss key leaf anatomical traits at the tissue, cellular, and sub-cellular level that influence the efficiency and effectiveness of C4 photosynthesis. Specifically, we discuss preconditioning of leaf traits that increase the evolvability of C4 photosynthesis, the evolutionary transition of organelles from C3 to a C4 leaf, gas and metabolite movement within the leaf, the positioning and maintenance of organelles in M and BS cells, and the movement of M chloroplasts.

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Abbreviations

ABA:

abscisic acid

A net :

net rate of CO2 assimilation

BS:

bundle-sheath

C2 :

plants using a photorespiratory glycine shuttle to concentrate CO2

C3 :

plants without a CO2 concentrating mechanism

C4 :

plants using a 4-carbon CO2 concentrating mechanism

CA:

carbonic anhydrase

C a :

CO2 partial in the atmosphere

CAM:

crassulacean acid metabolism

CCM:

CO2 concentrating mechanism

C i :

CO2 partial pressure in the intercellular air space

CO2 :

carbon dioxide

δ13C:

the carbon isotope composition

Δ13C:

carbon isotope discrimination

E :

transpiration

g b :

boundary layer conductance

g bs :

conductance of CO2 between the BS and M cells or the corresponding cellular compartments in the single-cell C4 system

GDC:

glycine decarboxylase complex

g m :

internal conductance of CO2 from the inter-cellular airspace to the initial site of carboxylation

g s :

stomatal conductance to either CO2 or H2O

HCO3 - :

bicarbonate

IVD:

inter-veinal distances

K leaf :

total leaf water conductance

K p :

Michaelis-Menten constant of PEPC for HCO3 -

M:

mesophyll

m:

mitochondrion

Myr:

million years

NADP-ME:

NADP-malic enzyme

NAD-ME:

NAD-malic enzyme

NH4 + :

ammonium

p:

peroxisome

PCK:

phosphoenolpyruvate carboxykinase

PD:

plasmodesmata

PEP:

phosphoenolpyruvate

PEPC:

phosphoenolpyruvate carboxylase

Ï• :

leakiness

S bs :

the BS surface area per unit leaf area

S m :

M surface area exposed to the inter-cellular air space

V:

vascular bundle

V pmax :

in vitro maximum PEPC activity

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Acknowledgments

The research of ABC was supported by the Office of Biological and Environmental Research in the DOE Office of Science (DE-SC0008769) and MT was supported by JSPS KAKENHI Grant Numbers JP26292011 and JP16K14835.

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Authors and Affiliations

  1. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Japan

    Mitsutaka Taniguchi

  2. School of Biological Sciences, Washington State University Pullman, Pullman, WA, USA

    Asaph B. Cousins

Authors
  1. Mitsutaka Taniguchi
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  2. Asaph B. Cousins
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Correspondence to Mitsutaka Taniguchi or Asaph B. Cousins .

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Editors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of Colorado, Boulder, CO, USA

    William W. Adams III

  2. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo Ku, Hongo, Tokyo, Japan

    Ichiro Terashima

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Taniguchi, M., Cousins, A.B. (2018). Significance of C4 Leaf Structure at the Tissue and Cellular Levels. In: Adams III, W., Terashima, I. (eds) The Leaf: A Platform for Performing Photosynthesis. Advances in Photosynthesis and Respiration, vol 44. Springer, Cham. https://doi.org/10.1007/978-3-319-93594-2_9

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