scholarly journals The role of photorespiration during the evolution of C4 photosynthesis in the genus Flaveria

eLife ◽  
2014 ◽  
Vol 3 ◽  
Author(s):  
Julia Mallmann ◽  
David Heckmann ◽  
Andrea Bräutigam ◽  
Martin J Lercher ◽  
Andreas PM Weber ◽  
...  

C4 photosynthesis represents a most remarkable case of convergent evolution of a complex trait, which includes the reprogramming of the expression patterns of thousands of genes. Anatomical, physiological, and phylogenetic and analyses as well as computational modeling indicate that the establishment of a photorespiratory carbon pump (termed C2 photosynthesis) is a prerequisite for the evolution of C4. However, a mechanistic model explaining the tight connection between the evolution of C4 and C2 photosynthesis is currently lacking. Here we address this question through comparative transcriptomic and biochemical analyses of closely related C3, C3–C4, and C4 species, combined with Flux Balance Analysis constrained through a mechanistic model of carbon fixation. We show that C2 photosynthesis creates a misbalance in nitrogen metabolism between bundle sheath and mesophyll cells. Rebalancing nitrogen metabolism requires anaplerotic reactions that resemble at least parts of a basic C4 cycle. Our findings thus show how C2 photosynthesis represents a pre-adaptation for the C4 system, where the evolution of the C2 system establishes important C4 components as a side effect.

2020 ◽  
Author(s):  
Soni Chowrasia ◽  
Tapan Kumar Mondal

AbstractThe C4 cycle is a complex biochemical pathway that has been evolved in plants to deal with the adverse environmental conditions. Mostly C4 plants grow in arid, water-logged area or poor nutrient habitats. Wild species, Oryza coarctata (genome type KKLL; chromosome number (4x) =48, genome size 665 Mb) belongs to the genus of Oryza which thrives well under high saline as well as submerged conditions. Here, we report for the first time that O. coarctata is a C4 plant by observing the increased biomass growth, morphological features such as vein density, anatomical features including ultrastuctural characteristics as well as expression patterns of C4 related genes. Leaves of O. coarctata have higher vein density and possess Kranz anatomy. The ultrastructural observation showed chloroplast dimorphism i.e. presence of agranal chloroplasts in bundle sheath cells whereas, mesophyll cells contain granal chloroplasts. The cell walls of bundle sheath cells contain tangential suberin lamella. The transcript level of C4 specific genes such as phosphoenolpyruvate carboxylase, pyruvate orthophosphate dikinase, NADP-dependent malic enzyme and malate dehydrogenase was higher in leaves of O. coarctata compare to high yielding rice cultivar (IR-29). These anatomical, ultra structural as well as molecular changes in O. coarctata for C4 photosynthesis adaptation might be might be due to its survival in wide diverse condition from aquatic to saline submerged condition. Being in the genus of Oryza, this plant could be potential donor for production of C4 rice in future through conventional breeding, as successful cross with rice has already been reported.


Author(s):  
Carla Coluccio Leskow ◽  
Mariana Conte ◽  
Talia del Pozo ◽  
Luisa Bermúdez ◽  
Bruno Silvestre Lira ◽  
...  

Abstract Sucrose metabolism is of high importance for most plant species, both as the main source of carbon and via signaling mechanisms that have been proposed for this molecule. Two cleaving enzymes channel sucrose into sink metabolism; sucrose synthases (SUS) and invertases (INV), which are localized in different subcellular compartments. Although acid soluble and insoluble invertases have been largely investigated, studies on the role of neutral invertases (A/N-INV) have lagged behind. Here, we identified a tomato A/N-INV encoding gene (NI6) co-localizing with a previously reported pathway QTL largely affecting primary carbon metabolism in tomato. Of the eight A/N-INV genes identified in the tomato genome, NI6 mRNA is present in all organs, but its expression was higher in sink tissues (mainly roots and fruits). A NI6-GFP fusion protein was found in the cytosol of mesophyll cells. Tomato NI6-silenced plants showed impaired growth phenotypes, delayed flowering and dramatic reduction in the fruit set. Global gene expression and metabolite profile analyses of these plants revealed that NI6 is not only essential for sugar metabolism but also plays a signaling role in stress adaptation. Gene-metabolite network analyses allowed identification of major hubs, whose expression patterns were greatly affected by NI6 silencing, within the signaling cascade that coordinates carbohydrate metabolism with growth and development in tomato.


2020 ◽  
Vol 71 (1) ◽  
pp. 183-215 ◽  
Author(s):  
Urte Schlüter ◽  
Andreas P.M. Weber

C4 photosynthesis evolved multiple times independently from ancestral C3 photosynthesis in a broad range of flowering land plant families and in both monocots and dicots. The evolution of C4 photosynthesis entails the recruitment of enzyme activities that are not involved in photosynthetic carbon fixation in C3 plants to photosynthesis. This requires a different regulation of gene expression as well as a different regulation of enzyme activities in comparison to the C3 context. Further, C4 photosynthesis relies on a distinct leaf anatomy that differs from that of C3, requiring a differential regulation of leaf development in C4. We summarize recent progress in the understanding of C4-specific features in evolution and metabolic regulation in the context of C4 photosynthesis.


2020 ◽  
Vol 71 (16) ◽  
pp. 4629-4638
Author(s):  
Sophie N R Young ◽  
Lawren Sack ◽  
Margaret J Sporck-Koehler ◽  
Marjorie R Lundgren

Abstract Since C4 photosynthesis was first discovered >50 years ago, researchers have sought to understand how this complex trait evolved from the ancestral C3 photosynthetic machinery on >60 occasions. Despite its repeated emergence across the plant kingdom, C4 photosynthesis is notably rare in trees, with true C4 trees only existing in Euphorbia. Here we consider aspects of the C4 trait that could limit but not preclude the evolution of a C4 tree, including reduced quantum yield, increased energetic demand, reduced adaptive plasticity, evolutionary constraints, and a new theory that the passive symplastic phloem loading mechanism observed in trees, combined with difficulties in maintaining sugar and water transport over a long pathlength, could make C4 photosynthesis largely incompatible with the tree lifeform. We conclude that the transition to a tree habit within C4 lineages as well as the emergence of C4 photosynthesis within pre-existing trees would both face a series of challenges that together explain the global rarity of C4 photosynthesis in trees. The C4 trees in Euphorbia are therefore exceptional in how they have circumvented every potential barrier to the rare C4 tree lifeform.


2020 ◽  
Vol 21 (3) ◽  
pp. 774
Author(s):  
Xuemei Xiao ◽  
Jian Lv ◽  
Jianming Xie ◽  
Zhi Feng ◽  
Ning Ma ◽  
...  

Autotoxicity of root exudates is one of the main reasons for consecutive monoculture problem (CMP) in cucumber under greenhouse cultivation. Rootstock grafting may improve the tolerance of cucumber plants to autotoxic stress. To verify the enhanced tolerance to autotoxic stress and illuminate relevant molecular mechanism, a transcriptomic comparative analysis was performed between rootstock grafted (RG) and non-grafted (NG) cucumber plants by a simulation of exogenous cinnamic acid (CA). The present study confirmed that relatively stable plant growth, biomass accumulation, chlorophyll content, and photosynthesis was observed in RG than NG under CA stress. We identified 3647 and 2691 differentially expressed genes (DEGs) in NG and RG cucumber plants when compared to respective control, and gene expression patterns of RNA-seq was confirmed by qRT-PCR. Functional annotations revealed that DEGs response to CA stress were enriched in pathways of plant hormone signal transduction, MAPK signaling pathway, phenylalanine metabolism, and plant-pathogen interaction. Interestingly, the significantly enriched pathway of photosynthesis-related, carbon and nitrogen metabolism only identified in NG, and most of DEGs were down-regulated. However, most of photosynthesis, Calvin cycle, glycolysis, TCA cycle, and nitrogen metabolism-related DEGs exhibited not or slightly down-regulated in RG. In addition, several stress-related transcription factor families of AP2/ERF, bHLH, bZIP, MYB. and NAC were uniquely triggered in the grafted cucumbers. Overall, the results of this study suggest that rootstock grafting improve the tolerance of cucumber plants to autotoxic stress by mediating down-regulation of photosynthesis, carbon, and nitrogen metabolism-related DEGs and activating the function of stress-related transcription factor. The transcriptome dataset provides an extensive sequence resource for further studies of autotoxic mechanism at molecular level.


eLife ◽  
2013 ◽  
Vol 2 ◽  
Author(s):  
Ben P Williams ◽  
Iain G Johnston ◽  
Sarah Covshoff ◽  
Julian M Hibberd

C4 photosynthesis has independently evolved from the ancestral C3 pathway in at least 60 plant lineages, but, as with other complex traits, how it evolved is unclear. Here we show that the polyphyletic appearance of C4 photosynthesis is associated with diverse and flexible evolutionary paths that group into four major trajectories. We conducted a meta-analysis of 18 lineages containing species that use C3, C4, or intermediate C3–C4 forms of photosynthesis to parameterise a 16-dimensional phenotypic landscape. We then developed and experimentally verified a novel Bayesian approach based on a hidden Markov model that predicts how the C4 phenotype evolved. The alternative evolutionary histories underlying the appearance of C4 photosynthesis were determined by ancestral lineage and initial phenotypic alterations unrelated to photosynthesis. We conclude that the order of C4 trait acquisition is flexible and driven by non-photosynthetic drivers. This flexibility will have facilitated the convergent evolution of this complex trait.


2018 ◽  
Author(s):  
Jenna C. Carlson ◽  
Deepti Anand ◽  
Azeez Butali ◽  
Carmen J. Buxo ◽  
Kaare Christensen ◽  
...  

AbstractPhenotypic heterogeneity is a hallmark of complex traits, and genetic studies of such traits may focus on them as a single diagnostic entity or by analyzing specific components. For example, in orofacial clefting (OFC), three subtypes – cleft lip (CL), cleft lip and palate (CLP), and cleft palate (CP) have been studied separately and in combination. To further dissect the genetic architecture of OFCs and how a given associated locus may be contributing to distinct subtypes of a trait we developed a framework for quantifying and interpreting evidence of subtype-specific or shared genetic effects in complex traits. We applied this technique to create a “cleft map” of the association of 30 genetic loci with three OFC subtypes. In addition to new associations, we found loci with subtype-specific effects (e.g., GRHL3 (CP), WNT5A (CLP)), as well as loci associated with two or all three subtypes. We cross-referenced these results with mouse craniofacial gene expression datasets, which identified additional promising candidate genes. However, we found no strong correlation between OFC subtypes and expression patterns. In aggregate, the cleft map revealed that neither subtype-specific nor shared genetic effects operate in isolation in OFC architecture. Our approach can be easily applied to any complex trait with distinct phenotypic subgroups.


2018 ◽  
Author(s):  
Po-Hsiang Wang ◽  
Kevin Correia ◽  
Han-Chen Ho ◽  
Naveen Venayak ◽  
Kayla Nemr ◽  
...  

AbstractMost microorganisms in the biosphere live in communities and develop coordinated metabolisms via trading metabolites. In this study, we sought to deconstruct the metabolic interdependency in organohalide-respiring microbial communities enriched withDehalobacter restrictus(Dhb), using a complementary approach of computational metabolic modeling and experimental validation.Dhbpossesses a complete set of genes for amino acid biosynthesis yet requires amino acid supplementation. We reconciled this discrepancy using Flux Balance Analysis with consideration for cofactor availability, enzyme promiscuity, and shared protein expression patterns of severalDhbstrains. Experimentally,13C incorporation assays, growth assays, and metabolite analysis of strain PER-K23 cultures were performed to validate the model predictions. The model resolved thatDhb’s amino acid dependency results from restricted NADPH regeneration and diagnosed that malate supplementation can replenish intracellular NADPH using malic enzyme. Interestingly, we observed unexpected export of glutamate and pyruvate in parallel to malate consumption in the strain PER-K23 cultures. Further experiments onDhb-enriched consortium ACT-3 suggested an interspecies malate-pyruvate shuttle betweenDhband a glutamate-auxotrophicBacteroidessp., reminiscent of the mitochondrial malate shunt pathway in eukaryotic cells. Altogether, this study reveals that redox constraints and metabolic complementarity are important driving forces for amino acid exchange in anaerobic microbial communities.


2021 ◽  
Author(s):  
Federico M. Ruiz ◽  
Sonia Huecas ◽  
Alicia Santos-Aledo ◽  
Elena A. Prim ◽  
José M. Andreu ◽  
...  

Treadmilling protein filaments perform essential cellular functions by growing from one end while shrinking from the other, driven by nucleotide hydrolysis. Bacterial cell division relies on the primitive tubulin homolog FtsZ, a target for antibiotic discovery that assembles into single treadmilling filaments that hydrolyse GTP at an active site formed upon subunit association. We determined high-resolution filament structures of FtsZ from the pathogen Staphylococcus aureus in complex with different nucleotide analogues and cations, including mimetics of the ground and transition states of catalysis. Together with mutational and biochemical analyses, our structures reveal interactions made by the GTP γ-phosphate and Mg2+ at the subunit interface, a K+ ion stabilizing loop T7 for co-catalysis, new roles of key residues at the active site and a nearby crosstalk area, and rearrangements of a dynamic water shell bridging adjacent subunits upon GTP hydrolysis. We propose a mechanistic model that integrates nucleotide hydrolysis signalling with assembly-associated conformational changes and filament treadmilling. Equivalent assembly mechanisms may apply to more complex tubulin and actin cytomotive filaments that share analogous features with FtsZ.


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