Quantitative Leaf Anatomy of C3 and C4 Grasses (Poaceae): Bundle Sheath and Mesophyll Surface Area Relationships

Dengler, Nancy G.; Dengler, Ronald E.; Donnelly, Petra M.; Hattersley, P. W.

doi:10.1006/anbo.1994.1029

Cited by 169 publications

(183 citation statements)

References 36 publications

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“…Similar to these results, no consistent differences were found in other comparisons of C 3 and C 4 species in the ability to reduce leaf thickness in response to shading (Sage and McKown 2006). Shorter intervenial distances we observed here for C 4 grasses than for C 3 grasses, and for C 4 NADP-ME species than for the C 4 NAD-ME C. dactylon are consistent with previous results (Dengler et al 1994, Kawamitsu et al 1985, Ogle 2003.…”

Section: Discussionsupporting

confidence: 92%

Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

Han

Mojzes

Kalapos

2008

Acta Botanica Hungarica

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Leaf morphology, coarse structure and anatomy were compared for two invasive C 4 , two non-invasive C 4 , and two expanding native C 3 grass species grown in their original, high-light semiarid temperate habitat, and in a growth room under variable moderate light and favourable supply of water and nutrients. It was hypothesised that (H 1 ) among C 4 grasses leaf structural response will be greater for invasive than for non-invasive species, and (H 2 ) for plants of high spreading capacity C 4 species will be less responsive than C 3 species. Leaf mass per area was lower in the growth room than in the field by 43.4-54% and 5.7-21.2% for grasses of high spreading capacity and for non-invasive C 4 species, respectively. Little or no response was observed in the proportion of epidermis and mesophyll, but the proportional area of veins plus sclerenchyma was greater in the field than in the growth room for the invasive C 4 Sorghum halepense, and the spreading C 3 Bromus inermis and Calamagrostis epigeios, while it did not differ for the two non-invasive C 4 grasses and the invasive C 4 Cynodon dactylon. Leaf intervenial distance was invariant for C 4 grasses (except for the non-invasive Chrysopogon gryllus) and the C 3 C. epigeios, but changed by 25.1% for the C 3 B. inermis. These results suggest that among C 4 grasses invasive species exceed non-invasive ones in the plasticity of leaf coarse structure, but not that of leaf morphology and anatomy. However, leaf structure was not less plastic in invasive C 4 than in expanding C 3 grasses except for intervenial distance.

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Section: Discussionsupporting

confidence: 92%

Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

Han

Mojzes

Kalapos

2008

Acta Botanica Hungarica

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“…Measurements of vein density in a range of C 3 and C 4 species demonstrated that veins are consistently more closely spaced in C 4 species (Crookston and Moss, 1974). Furthermore, quantitative measurements of BS-to-M cell ratios in C 3 and C 4 leaves showed that in C 4 plants the ratio approaches 1:1 (Hattersley and Watson, 1975;Dengler et al, 1994;Muhaidat et al, 2007). This ratio equates to veins (V) being separated by only four photosynthetic cells in C 4 leaves as opposed to up to 20 cells in C 3 leaves ( Figure 3).…”

Section: Veins Act As Organizing Centersmentioning

confidence: 99%

C₄ Cycles: Past, Present, and Future Research on C₄ Photosynthesis

2011

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In the late 1960s, a vibrant new research field was ignited by the discovery that instead of fixing CO 2 into a C 3 compound, some plants initially fix CO 2 into a four-carbon (C 4 ) compound. The term C 4 photosynthesis was born. In the 20 years that followed, physiologists, biochemists, and molecular and developmental biologists grappled to understand how the C 4 photosynthetic pathway was partitioned between two morphologically distinct cell types in the leaf. By the early 1990s, much was known about C 4 biochemistry, the types of leaf anatomy that facilitated the pathway, and the patterns of gene expression that underpinned the biochemistry. However, virtually nothing was known about how the pathway was regulated. It should have been an exciting time, but many of the original researchers were approaching retirement, C 4 plants were proving recalcitrant to genetic manipulation, and whole-genome sequences were not even a dream. In combination, these factors led to reduced funding and the failure to attract young people into the field; the endgame seemed to be underway. But over the last 5 years, there has been a resurgence of interest and funding, not least because of ambitious multinational projects that aim to increase crop yields by introducing C 4 traits into C 3 plants. Combined with new technologies, this renewed interest has resulted in the development of more sophisticated approaches toward understanding how the C 4 pathway evolved, how it is regulated, and how it might be manipulated. The extent of this resurgence is manifest by the publication in 2011 of more than 650 pages of reviews on different aspects of C 4 . Here, I provide an overview of our current understanding, the questions that are being addressed, and the issues that lie ahead.

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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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Quantitative Leaf Anatomy of C3 and C4 Grasses (Poaceae): Bundle Sheath and Mesophyll Surface Area Relationships

Cited by 169 publications

References 36 publications

Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

C₄ Cycles: Past, Present, and Future Research on C₄ Photosynthesis

Anatomical enablers and the evolution of C ₄ photosynthesis in grasses

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Quantitative Leaf Anatomy of C3 and C4 Grasses (Poaceae): Bundle Sheath and Mesophyll Surface Area Relationships

Cited by 169 publications

References 36 publications

Leaf morphology and anatomy in two contrasting environments for C3and C4grasses of different invasion potential

Leaf morphology and anatomy in two contrasting environments for C3and C4grasses of different invasion potential

C4 Cycles: Past, Present, and Future Research on C4 Photosynthesis

Anatomical enablers and the evolution of C 4 photosynthesis in grasses

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Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

Leaf morphology and anatomy in two contrasting environments for C₃and C₄grasses of different invasion potential

C₄ Cycles: Past, Present, and Future Research on C₄ Photosynthesis

Anatomical enablers and the evolution of C ₄ photosynthesis in grasses