Understanding the Genetic Basis of C<sub>4</sub> Kranz Anatomy with a View to Engineering C<sub>3</sub> Crops

Sedelnikova, Olga V.; Hughes, Thomas E; Langdale, Jane A.

doi:10.1146/annurev-genet-120417-031217

Cited by 91 publications

(75 citation statements)

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“…The C4 photosynthetic pathway, which is responsible for around 21% of global primary productivity 35 despite being found in only ~3% of plant species (Ehleringer et al, 1997;Sage et al, 2011), is 36 underpinned by a specialized leaf anatomy known as Kranz (the German word for wreath) (reviewed 37 in Sedelnikova et al, 2018). Unlike in C3 plants, where photosynthesis only occurs in the mesophyll 38 cells, the C4 pathway is separated between bundle sheath (BS) and mesophyll (M) cells, with the 39 two cell-types forming concentric wreaths around leaf veins (reviewed in Langdale, 2011).…”

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RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

Hughes

Sedelnikova

et al. 2019

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16 17 Summary statement: Two duplicated maize SCARECROW genes control the development of the 18 endodermis in roots and the mesophyll in leaves 19 2 ABSTRACT 20 The highly efficient C4 photosynthetic pathway is facilitated by 'Kranz' leaf anatomy. In Kranz leaves, 21 closely spaced veins are encircled by concentric layers of photosynthetic bundle sheath (inner) and 22 65 recruited in the leaf rather than the root in maize, but the subtle phenotype reported in leaves of 66 Zmscr1 mutants precludes an understanding of the precise role played during Kranz development. 67 68 Both gene and whole genome duplication events are highly prevalent throughout the plant phylogeny 69 (Adams and Wendel, 2005; Blanc and Wolfe, 2004) and if retained in the genome, duplicated genes 70 are free to sub-or neo-functionalize (Moore and Purugganan, 2005; Ohno, 1970). Perhaps more 71 553 Adams, K. L. and Wendel, J. F. (2005). Polyploidy and genome evolution in plants. Curr. Opin.

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RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

Hughes

Sedelnikova

et al. 2019

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“…The insertion of minor veins could occur via relatively few developmental changes, likely underpinned by changes to auxin, brassinosteroids, SHORTROOT/SCARECROW and/or INDETERMINATE DOMAIN transcription factors (Kumar & Kellogg ; Sedelnikova et al . ). In grasses, vein orders develop sequentially as leaves grow wider, such that minor veins are initiated considerably later than other vein orders, usually once the leaf ceases to widen (Nelson & Langdale ; Sedelnikova et al .…”

Section: Discussionmentioning

confidence: 97%

“…In grasses, vein orders develop sequentially as leaves grow wider, such that minor veins are initiated considerably later than other vein orders, usually once the leaf ceases to widen (Nelson & Langdale ; Sedelnikova et al . ). Thus, the development of functional minor veins likely arises via the heterochronic regulation of the existing machinery for vein formation, sustaining vein differentiation beyond that of non‐C 4 plants (Nelson ; Sedelnikova et al .…”

Section: Discussionmentioning

confidence: 97%

“…Thus, the development of functional minor veins likely arises via the heterochronic regulation of the existing machinery for vein formation, sustaining vein differentiation beyond that of non‐C 4 plants (Nelson ; Sedelnikova et al . ), probably through the prolonged production of auxin during later phases of leaf elongation (Scarpella et al . ).…”

Section: Discussionmentioning

confidence: 99%

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C₄ anatomy can evolve via a single developmental change

et al. 2018

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C4 photosynthesis is a complex trait that boosts productivity in warm environments. Paradoxically, it evolved independently in numerous plant lineages, despite requiring specialised leaf anatomy. The anatomical modifications underlying C4 evolution have previously been evaluated through interspecific comparisons, which capture numerous changes besides those needed for C4 functionality. Here, we quantify the anatomical changes accompanying the transition between non‐C4 and C4 phenotypes by sampling widely across the continuum of leaf anatomical traits in the grass Alloteropsis semialata. Within this species, the only trait that is shared among and specific to C4 individuals is an increase in vein density, driven specifically by minor vein development that yields multiple secondary effects facilitating C4 function. For species with the necessary anatomical preconditions, developmental proliferation of veins can therefore be sufficient to produce a functional C4 leaf anatomy, creating an evolutionary entry point to complex C4 syndromes that can become more specialised.

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“…They either analyzed the ontogeny of whole leaves (Wang et al, 2013a; Külahoglu et al, 2014) or sections of leaves that covered different stages of development (Aubry et al, 2014; Kümpers et al, 2017). Combined with in-depth analyses of several candidate genes, these approaches provided some insights into the changes of leaf development during C 4 evolution as reviewed recently in (Sedelnikova et al, 2018) and (Kumar and Kellogg, 2018).…”

Section: Introductionmentioning

confidence: 99%

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy

Billakurthi

Wrobel

Bräutigam

et al. 2018

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C4 species have evolved more than 60 times independently from C3 ancestors. This multiple and parallel evolution of the complex C4 trait indicates common underlying evolutionary mechanisms that might be identified by comparative analysis of closely related C3 and C4 species. Efficient C4 function depends on a distinctive leaf anatomy that is characterized by enlarged, chloroplast rich bundle sheath cells and a narrow vein spacing. To elucidate molecular mechanisms generating this so called Kranz anatomy, we analyzed a developmental series of leaves from the C4 plant Flaveria bidentis and the closely related C3 species Flaveria robusta using leaf clearing and whole transcriptome sequencing. Applying non-negative matrix factorization on the data identified four different zones with distinct transcriptome patterns in growing leaves of both species. Comparing these transcriptome patterns revealed an important role of auxin metabolism and especially auxin homeostasis for establishing the high vein density typical for C4 leaves.2012). Under current ambient CO2 concentrations (405 ppm) at 25°C, photorespiration is estimated to decrease the yield of soybean or wheat in the US by 36% and 20%, respectively (Walker et al., 2016). Environmental constrains such as high temperatures and drought further increases Rubisco oxygenase activity (Laing et al., 1974; Jordan and Ogren, 1984; Brooks and Farquhar, 1985; Parry et al., 2007).In most C4 plants CO2 fixation is compartmentalized between two cell types, the bundle sheath (BS) and the mesophyll (M) cells. In the mesophyll phosphoenolpyruvate (PEP) is carboxylated by phosphoenolpyruvate carboxylase (PEPC), resulting in the 4-carbon compound oxaloacetate (OAA). OAA is converted to malate and/or aspartate, which is then transferred to the bundle sheath. Here the 4-carbon compounds are decarboxylated and the released CO2 is assimilated in the Calvin-Benson-Bassham cycle (CBB). The resulting pyruvate is transferred back to the mesophyll where the primary CO2 acceptor PEP is regenerated by pyruvate orthophosphate dikinase (PPDK) (Hatch, 1987).C4 photosynthesis requires a particular leaf anatomy. As BS and M cells operate as a photosynthetic unit, direct contact of both cell types is necessary to ensure efficient photosynthesis.The BS is composed of the cells directly adjacent to the vasculature. Therefore, leaves of most C4 species exhibit high vein densities with a characteristic pattern in which two veins, each surrounded by BS cells, are separated by only two layers of M cells in a vein-bundle sheathmesophyll-mesophyll-bundle sheath-vein layout. Bundle sheath cells of C4 plants often appear larger in cross-section compared to C3 species and contain more chloroplasts. This character-

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Understanding the Genetic Basis of C₄ Kranz Anatomy with a View to Engineering C₃ Crops

Cited by 91 publications

References 152 publications

RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

C₄ anatomy can evolve via a single developmental change

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy

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Understanding the Genetic Basis of C4 Kranz Anatomy with a View to Engineering C3 Crops

Cited by 91 publications

References 152 publications

RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

RedundantSCARECROWgenes pattern distinct cell layers in roots and leaves of maize

C4 anatomy can evolve via a single developmental change

Transcriptome dynamics in developing leaves from C3and C4Flaveriaspecies reveal determinants of Kranz anatomy

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Understanding the Genetic Basis of C₄ Kranz Anatomy with a View to Engineering C₃ Crops

C₄ anatomy can evolve via a single developmental change

Transcriptome dynamics in developing leaves from C₃and C₄Flaveriaspecies reveal determinants of Kranz anatomy