Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy

Koteyeva, Nuria K.; Voznesenskaya, Elena V.; Edwards, Gerald E.

doi:10.1093/jxb/eru042

Cited by 25 publications

(36 citation statements)

References 62 publications

(148 reference statements)

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“…Similar gradients in leaf maturation have recently been reported in both C. gynandra and Cleome angustifolia , and immunolocalisation showed selective localisation of RuBisCO in chloroplasts of the BS prior to structural differentiation of M and BS cells [24]. This suggests in C. gynandra , trans -acting factors which are selectively expressed in M or BS cells, and which appear early in the basal section of the leaf, may be candidates for cell specific control of synthesis of some C 4 enzymes [24], [40]. Equivalent gradients in gene expression are detected along ∼10 cm of maize leaf.…”

Section: Discussionsupporting

confidence: 84%

“…In maize 21–25% of all genes expressed in leaves were estimated to be differentially expressed in M and BS cells [13], [24]. As these maize experiments were conducted with very different technologies there are significant differences in their estimates of gene expression, however we found 1,154 and 1,429 genes that were preferentially expressed in the M or BS respectively in both maize datasets.…”

Section: Discussionmentioning

confidence: 69%

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Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis

et al. 2014

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With at least 60 independent origins spanning monocotyledons and dicotyledons, the C4 photosynthetic pathway represents one of the most remarkable examples of convergent evolution. The recurrent evolution of this highly complex trait involving alterations to leaf anatomy, cell biology and biochemistry allows an increase in productivity by ∼50% in tropical and subtropical areas. The extent to which separate lineages of C4 plants use the same genetic networks to maintain C4 photosynthesis is unknown. We developed a new informatics framework to enable deep evolutionary comparison of gene expression in species lacking reference genomes. We exploited this to compare gene expression in species representing two independent C4 lineages (Cleome gynandra and Zea mays) whose last common ancestor diverged ∼140 million years ago. We define a cohort of 3,335 genes that represent conserved components of leaf and photosynthetic development in these species. Furthermore, we show that genes encoding proteins of the C4 cycle are recruited into networks defined by photosynthesis-related genes. Despite the wide evolutionary separation and independent origins of the C4 phenotype, we report that these species use homologous transcription factors to both induce C4 photosynthesis and to maintain the cell specific gene expression required for the pathway to operate. We define a core molecular signature associated with leaf and photosynthetic maturation that is likely shared by angiosperm species derived from the last common ancestor of the monocotyledons and dicotyledons. We show that deep evolutionary comparisons of gene expression can reveal novel insight into the molecular convergence of highly complex phenotypes and that parallel evolution of trans-factors underpins the repeated appearance of C4 photosynthesis. Thus, exploitation of extant natural variation associated with complex traits can be used to identify regulators. Moreover, the transcription factors that are shared by independent C4 lineages are key targets for engineering the C4 pathway into C3 crops such as rice.

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Section: Discussionsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 69%

Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis

et al. 2014

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“…By contrast with grasses, our knowledge on the ontogeny of the bundle sheath in dicots is limited. It has been reported that the bundle sheaths of C 3 and C 4 Cleome species, originate from more than one layer of ground meristem cells and only adaxial bundle sheath cells are of procambial origin (Koteyeva et al ., ). As the bundle sheath and vascular tissue either completely or partially arise from the same cell lineage, changes in the vascular tissue might subsequently result in changes in the bundle sheath anatomy as well.…”

Section: Discussionmentioning

confidence: 97%

Reporter‐based forward genetic screen to identify bundle sheath anatomy mutants in A. thaliana

et al. 2019

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SummaryThe evolution of C4 photosynthesis proceeded stepwise with each small step increasing the fitness of the plant. An important pre‐condition for the introduction of a functional C4 cycle is the photosynthetic activation of the C3 bundle sheath by increasing its volume and organelle number. Therefore, to engineer C4 photosynthesis into existing C3 crops, information about genes that control the bundle sheath cell size and organelle content is needed. However, very little information is known about the genes that could be manipulated to create a more C4–like bundle sheath. To this end, an ethylmethanesulfonate (EMS)‐based forward genetic screen was established in the Brassicaceae C3 species Arabidopsis thaliana. To ensure a high‐throughput primary screen, the bundle sheath cells of A. thaliana were labeled using a luciferase (LUC68) or by a chloroplast‐targeted green fluorescent protein (sGFP) reporter using a bundle sheath specific promoter. The signal strengths of the reporter genes were used as a proxy to search for mutants with altered bundle sheath anatomy. Here, we show that our genetic screen predominantly identified mutants that were primarily affected in the architecture of the vascular bundle, and led to an increase in bundle sheath volume. By using a mapping‐by‐sequencing approach the genomic segments that contained mutated candidate genes were identified.

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“…All forms of C 4 species studied so far have been observed with the gradient differentiation of the photosynthetic structure and biochemistry, which finally results in establishment of a fully functional C 4 syndrome (Koteyeva et al, 2014;Koteyeva et al, 2016). In the Kranz-type C 4 species representatives, maize and Arundinella hirta in the Poaceae, the latter has not only M and BS cells (normal Kranz cells) but also another type of Kranz cells (named as distinctive [D] cells), which are not associated with vascular bundles (VB); however, all cell types show progressive differentiation and enzyme induction pattern, i.e.…”

Section: Introductionmentioning

confidence: 99%

“…In coordination with formation of Kranz anatomy, the chloroplast dimorphism and mitochondrial differentiation are established, and the expression of PPDK, NAD-malic enzyme (NAD-ME), RUBPC, or PEPC is significantly increased in parallel (Koteyeva et al, 2011a). Different types of anatomy between Cleome angustifolia and Cleome gynandra (with single and multiple Kranz units, respectively) suggest the independent evolutionary origins of C 4 photosynthesis, but they present similar developmental enhancement of C 4 system (Koteyeva et al, 2014). In SC-C 4 species S. aralocaspica and B. sinuspersici, a gradual enhancement of development along a longitudinal gradient of the young leaf is accompanied by increasing activity of photosynthetic enzymes (e.g.…”

Section: Introductionmentioning

confidence: 99%

The Developmental Enhancement of a C4 System With Non-Typical C4 Physiological Characteristics in Salsola ferganica (Kranz Anatomy), an Annual Desert Halophyte

et al. 2020

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Variations of photosynthetic structures in different tissues or cells are in coordination with changes in various aspects, e.g. physiology, biochemistry, gene expression, etc. Most C 4 plant species undergo developmental enhancement of the photosynthetic system, which may present different modes of changes between anatomy and physiology/biochemistry. In the current study, we investigated a Kranz-type C 4 species Salsola ferganica with the progressive development of photosynthetic (PS) structure, performance of PS physiology, induction of PS enzymes, and transcriptional and translational regulation of PS genes, results revealed that S. ferganica presented C 3 type anatomy in cotyledons but C 4 type in leaves (C 3 /L 4), with the C 4 system separation of initial carbon fixation in the palisade mesophyll (M) cells and the following incorporation into triosephosphates and sugars in the bundle sheath (BS) cells, respectively. The BS cells continuously surrounded the vascular bundles and water storage cells in leaf anatomic structure. Compared to the single-cell C 4 species Suaeda aralocaspica, S. ferganica exhibited similar developmental enhancement of C 4 syndrome temporally and spatially in anatomic structures, enzyme activities, and gene expression, which suggests that completion of differentiation of the photosynthetic system is necessary for a C 4 assimilation pathway. Besides, S. ferganica also displayed some different characteristics compared to S. aralocaspica in photosynthetic physiology, e.g. a more flexible d 13 C value, much lower phosphoenolpyruvate carboxylase (PEPC) activity, and an insensitive response to stimuli, etc., which were not typical C 4 characteristics. We speculate that this may suggest a different status of these two species in the evolutionary process of the photosynthesis pathway. Our findings will contribute to further understanding of the diversity of photosynthesis systems in Kranz-type C 4 species and the Salsola genus.

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Differentiation of C4 photosynthesis along a leaf developmental gradient in two Cleome species having different forms of Kranz anatomy

Abstract: SummaryIn Cleome species (Cleomaceae) having two different forms and evolutionary origins of Kranz anatomy there is convergence in the structural and biochemical expression of C4 traits during leaf ontogeny.

Cited by 25 publications

References 62 publications

Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis

Deep Evolutionary Comparison of Gene Expression Identifies Parallel Recruitment of Trans-Factors in Two Independent Origins of C4 Photosynthesis

Reporter‐based forward genetic screen to identify bundle sheath anatomy mutants in A. thaliana

The Developmental Enhancement of a C4 System With Non-Typical C4 Physiological Characteristics in Salsola ferganica (Kranz Anatomy), an Annual Desert Halophyte

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