Leaf Structure and Development in C4 Plants

Dengler, Nancy G.; Nelson, Timothy

doi:10.1016/b978-012614440-6/50006-9

Cited by 181 publications

(202 citation statements)

References 145 publications

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“…Although several examples of C 4 photosynthesis operating in single cells have been described (Reiskind et al, 1997;Casati et al, 2000;Reinfelder et al, 2000;Voznesenskaya et al, 2002Voznesenskaya et al, , 2003, most C 4 species compartmentalize carboxylation and decarboxylation activities into two distinct cell types. At least 22 variations of two-celled "Kranz" anatomy have been documented (Dengler and Nelson, 1999;Edwards and Voznesenskaya, 2011;Sage et al, 2012) whereby different cell types have been coopted as the photosynthetic carbon assimilation and photosynthetic carbon reduction tissue. In the grasses, nine types of Kranz anatomy have been described (Edwards and Voznesenskaya, 2011).…”

mentioning

confidence: 99%

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

et al. 2012

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C4 photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, cell biology, and development of leaves. The characteristic “Kranz” anatomy of most C4 leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C4) chromosomes to be investigated in an oat (Avena sativa; C3) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C4 characteristics into oat and have associated any C4-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C4 biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C3 oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2′-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger bundle sheath cells with increased cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C4 biology could be integrated into leaves of C3 crops.

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confidence: 99%

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

et al. 2012

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“…Such enablers may include ecological factors, as well as genomic and anatomical properties (10). For optimal functioning of the C 4 pathway, foliar anatomy must be altered to increase the relative proportion of BS cells and reduce the average path length between M and BS cells (12)(13)(14)(15). These modifications guarantee an efficient centripetal increase of CO 2 concentration, but they also imply that C 4 evolution involved many mutations, unless the C 3 ancestors already possessed some C 4 -like anatomical characters.…”

mentioning

confidence: 99%

Anatomical enablers and the evolution of C ₄ photosynthesis in grasses

Christin

Osborne

Chatelet

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

239

254

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C 4 photosynthesis is a series of anatomical and biochemical modifications to the typical C 3 pathway that increases the productivity of plants in warm, sunny, and dry conditions. Despite its complexity, it evolved more than 62 times independently in flowering plants. However, C 4 origins are absent from most plant lineages and clustered in others, suggesting that some characteristics increase C 4 evolvability in certain phylogenetic groups. The C 4 trait has evolved 22-24 times in grasses, and all origins occurred within the PACMAD clade, whereas the similarly sized BEP clade contains only C 3 taxa. Here, multiple foliar anatomy traits of 157 species from both BEP and PACMAD clades are quantified and analyzed in a phylogenetic framework. Statistical modeling indicates that C 4 evolvability strongly increases when the proportion of vascular bundle sheath (BS) tissue is higher than 15%, which results from a combination of short distance between BS and large BS cells. A reduction in the distance between BS occurred before the split of the BEP and PACMAD clades, but a decrease in BS cell size later occurred in BEP taxa. Therefore, when environmental changes promoted C 4 evolution, suitable anatomy was present only in members of the PACMAD clade, explaining the clustering of C 4 origins in this lineage. These results show that key alterations of foliar anatomy occurring in a C 3 context and preceding the emergence of the C 4 syndrome by millions of years facilitated the repeated evolution of one of the most successful physiological innovations in angiosperm history.precursor | preadaptation | phylogeny | Poaceae

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“…CO 2 leakage is described also as a diffusion process with a diffusion coefficient in the cytosol of 1.7 3 10 29 m 2 s 21 (Evans et al, 2009). Apoplastic diffusion of CO 2 is not considered because the outer cell wall of the BSCs of NADP-ME plants usually includes a suberin band, which effectively eliminates apoplastic leakage of CO 2 (Dengler and Nelson, 1999). CO 2 flux across the BSC chloroplast envelopes is simulated as a simple diffusion process with a permeability coefficient of 2 3 10 25 m s 21 (Uehlein et al, 2008;Evans et al, 2009;Supplemental Fig.…”

Section: Rate Equationsmentioning

confidence: 99%

Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis

2014

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C4 photosynthesis has higher light, nitrogen, and water use efficiencies than C3 photosynthesis. Although the basic anatomical, cellular, and biochemical features of C4 photosynthesis are well understood, the quantitative significance of each element of C4 photosynthesis to the high photosynthetic efficiency are not well defined. Here, we addressed this question by developing and using a systems model of C4 photosynthesis, which includes not only the Calvin-Benson cycle, starch synthesis, sucrose synthesis, C4 shuttle, and CO 2 leakage, but also photorespiration and metabolite transport between the bundle sheath cells and mesophyll cells. The model effectively simulated the CO 2 uptake rates, and the changes of metabolite concentrations under varied CO 2 and light levels. Analyses show that triose phosphate transport and CO 2 leakage can help maintain a high photosynthetic rate by balancing ATP and NADPH amounts in bundle sheath cells and mesophyll cells. Finally, we used the model to define the optimal enzyme properties and a blueprint for C4 engineering. As such, this model provides a theoretical framework for guiding C4 engineering and studying C4 photosynthesis in general.

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Leaf Structure and Development in C4 Plants

Cited by 181 publications

References 145 publications

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Anatomical enablers and the evolution of C ₄ photosynthesis in grasses

Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis

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Leaf Structure and Development in C4 Plants

Cited by 181 publications

References 145 publications

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

Anatomical enablers and the evolution of C 4 photosynthesis in grasses

Elements Required for an Efficient NADP-Malic Enzyme Type C4 Photosynthesis

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Anatomical enablers and the evolution of C ₄ photosynthesis in grasses