scholarly journals Changes in the plasmodesma structure and permeability at the bundle sheath and mesophyll interface during the maize C4 leaf development

2020 ◽  
Author(s):  
Peng Gao ◽  
Baijuan Du ◽  
Pinghua Li ◽  
Byung-Ho Kang
Keyword(s):  
Cell Wall ◽  
Organic Acids ◽  
Molecular Diffusion ◽  
C4 Photosynthesis ◽  
Solute Concentration ◽  
Bundle Sheath ◽  
Solute Diffusion ◽  
Cell Wall Modification ◽  
Maize Leaf ◽  
Kranz Anatomy

AbstractPlasmodesmata are intercellular channels that facilitate molecular diffusion between neighboring plant cells. The development and functions of plasmodesmata are controlled by multiple intra- and intercellular signaling pathways. Plasmodesmata are critical for dual-cell C4 photosynthesis in maize because plasmodesmata at the mesophyll and bundle sheath interface mediate exchange of CO2-carrying organic acids. We examined developmental profiles of plasmodesmata and chloroplasts in the maize leaf from young cells in the base to mature cell in the tip using microscopy approaches. Young mesophyll and bundle sheath cells in the leaf base had proplastids, and their plasmodesmata were simple, devoid of cytoplasmic sleeves. In maturing cells where Kranz anatomy and dimorphic chloroplasts were evident, we observed extensive remodeling of plasmodesmata that included acquisition of an electron-dense ring on the mesophyll side and cytoplasmic sleeves on the bundle sheath side. Interestingly, the changes in plasmodesmata involved a drop in symplastic dye mobility and suberin accumulation in the cell wall, implying a more stringent mesophyll-bundle sheath transport. We compared kinetics of the plasmodesmata and the cell wall modification in wildtype leaves with leaves from ppdk and dct2 mutants with defective C4 pathways. Plasmodesmata development, symplastic transport inhibition, and cell wall suberization were accelerated in the mutant lines, probably due to the aberrant C4 cycle. Transcriptomic analyses of the mutants confirmed the expedited changes in the cell wall. Our results suggest that a regulatory machinery at the mesophyll-bundle sheath boundary suppresses erroneous flux of C4 metabolites in the maize leaf.Significance StatementPlasmodesmata in the maize Kranz anatomy mediate the exchange of organic acids between mesophyll and bundle sheath. Since solute diffusion through plasmodesmata is governed by solute concentration gradients, a balanced distribution of C4 metabolites is critical for concentration of CO2 in the bundle sheath. Plasmodesmata bridging the mesophyll and bundle sheath cytoplasm have a cylindrical cavity, which can facilitate molecular movements, and a valve-like attachment. Construction of the sophisticated plasmodesmata was linked to C4 photosynthesis, and plasmodesmata assembly finished more rapidly in maize mutants with defective C4 pathways than in wild-type plants. These results suggest that the specialized plasmodesmata contribute to controlled transport of C4 metabolites.

scholarly journals Accelerated remodeling of the mesophyll-bundle sheath interface in the maize C4 cycle mutant leaves

2021 ◽  
Author(s):  
Peng Gao ◽  
Pengfei Wang ◽  
Baijuan Du ◽  
Pinghua Li ◽  
Byung-Ho Kang
Keyword(s):  
Cell Wall ◽  
Organic Acids ◽  
C4 Photosynthesis ◽  
Bundle Sheath ◽  
Wild Type ◽  
Symplastic Transport ◽  
Maize Leaf ◽  
Kranz Anatomy ◽  
Chloroplast Differentiation ◽  
Kinetics Of

Abstract C4 photosynthesis in the maize leaf involves the exchange of organic acids between mesophyll (M) and the bundle sheath (BS) cells. The transport is mediated by plasmodesmata embedded in the suberized cell wall. We examined the maize Kranz anatomy with a focus on the plasmodesma and cell wall suberization with microscopy methods. In the young leaf zone where M and BS cells had indistinguishable proplastids, plasmodesmata were simple and no suberin was detected. In leaf zones where dimorphic chloroplasts were evident, the plasmodesma acquired sphincter and cytoplasmic sleeves, and suberin was discerned. These modifications were accompanied by a drop in symplastic dye mobility at the M-BS boundary. We compared the kinetics of chloroplast differentiation and the modifications in M-BS connectivity in ppdk and dct2 mutants where C4 cycle is affected. The rate of chloroplast diversification did not alter, but plasmodesma remodeling, symplastic transport inhibition, and cell wall suberization were observed from younger leaf zone in the mutants than in wild type. Our results indicate that inactivation of the C4 genes accelerated the changes in the M-BS interface and the reduced permeability suggests that symplastic transport between M and BS could be gated probably for suppressing erroneous flux of C4 metabolites.

scholarly journals LEAF ANATOMY CHARACTERIZATION OF FOUR Apochloa SPECIES: A C3 GENUS RELATED TO EVOLUTION OF C4 PATHWAY IN GRASSES

2020 ◽  
Vol 26 (1) ◽  
pp. 12-18
Author(s):  
Ane Marcela das Chagas Mendonça ◽  
Pedro Lage Viana ◽  
João Paulo Rodrigues Alves Delfino Barbosa
Keyword(s):  
Leaf Anatomy ◽  
C4 Photosynthesis ◽  
Water Status ◽  
Bundle Sheath ◽  
C3 Plants ◽  
Plant Water ◽  
Kranz Anatomy ◽  
C4 Pathway ◽  
Photosynthesis Pathway

Leaf anatomy characteristics provide important evidences about the transition between C3 and C4 pathways. The C4 photosynthesis pathway allowed to reduce the C3 photorespiratory rate, concentrating CO2 around the Rubisco site and using structures and machinery already presented in C3 plants. In monocots, it is observed a high number of C4 lineages, most of them phylogenetically related to C3 groups. The genus Apochloa (C3), subtribe Arthropogoninae, is related to two C4 genera Coleataenia and Cyphonanthus. The aim of this study was to evaluate four Apochloa species in order to establish anatomical characteristics related to the evolution of C4 pathway in this group. By means of transverse sections fully expanded leaves of A. euprepes, A. lorea, A. molinioides, and A. poliophylla were collected and the characteristics of the mesophyll (M) and bundle sheath (BS) cells were determined. These species showed a rustic Kranz anatomy with enlarged and radial arranged BS cells, which have few organelles organized in a centrifugal position. Although the modifications of BS cells are probably related to the maintenance of plant water status, we also discuss the evolution for the establishment of C4 photosynthesis in the related C4 genera.

scholarly journals Challenges and Approaches to Crop Improvement Through C3-to-C4 Engineering

2021 ◽  
Vol 12 ◽  
Author(s):  
Hongchang Cui
Keyword(s):  
Photosynthetic Efficiency ◽  
C4 Photosynthesis ◽  
Crop Improvement ◽  
Bundle Sheath ◽  
C4 Plants ◽  
System Level ◽  
C3 Plants ◽  
World Population ◽  
Kranz Anatomy ◽  
The Past

With a rapidly growing world population and dwindling natural resources, we are now facing the enormous challenge of increasing crop yields while simultaneously improving the efficiency of resource utilization. Introduction of C4 photosynthesis into C3 crops is widely accepted as a key strategy to meet this challenge because C4 plants are more efficient than C3 plants in photosynthesis and resource usage, particularly in hot climates, where the potential for productivity is high. Lending support to the feasibility of this C3-to-C4 engineering, evidence indicates that C4 photosynthesis has evolved from C3 photosynthesis in multiple lineages. Nevertheless, C3-to-C4 engineering is not an easy task, as several features essential to C4 photosynthesis must be introduced into C3 plants. One such feature is the spatial separation of the two phases of photosynthesis (CO2 fixation and carbohydrate synthesis) into the mesophyll and bundle sheath cells, respectively. Another feature is the Kranz anatomy, characterized by a close association between the mesophyll and bundle sheath (BS) cells (1:1 ratio). These anatomical features, along with a C4-specific carbon fixation enzyme (PEPC), form a CO2-concentration mechanism that ensures a high photosynthetic efficiency. Much effort has been taken in the past to introduce the C4 mechanism into C3 plants, but none of these attempts has met with success, which is in my opinion due to a lack of system-level understanding and manipulation of the C3 and C4 pathways. As a prerequisite for the C3-to-C4 engineering, I propose that not only the mechanisms that control the Kranz anatomy and cell-type-specific expression in C3 and C4 plants must be elucidated, but also a good understanding of the gene regulatory network underlying C3 and C4 photosynthesis must be achieved. In this review, I first describe the past and current efforts to increase photosynthetic efficiency in C3 plants and their limitations; I then discuss a systems approach to tackling down this challenge, some practical issues, and recent technical innovations that would help us to solve these problems.

scholarly journals C4 photosynthesis with Kranz anatomy evolved in the Oryza coarctata Roxb

2020 ◽  
Author(s):  
Soni Chowrasia ◽  
Tapan Kumar Mondal
Keyword(s):  
C4 Photosynthesis ◽  
Expression Patterns ◽  
Bundle Sheath ◽  
Ultrastructural Observation ◽  
Mesophyll Cells ◽  
Potential Donor ◽  
Kranz Anatomy ◽  
Vein Density ◽  
Bundle Sheath Cells ◽  
Sheath Cells

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.

scholarly journals Bundle sheath suberisation is required for C4 photosynthesis in a Setaria viridis mutant

2021 ◽  
Vol 4 (1) ◽  
Author(s):  
Florence R. Danila ◽  
Vivek Thakur ◽  
Jolly Chatterjee ◽  
Soumi Bala ◽  
Robert A. Coe ◽  
...  
Keyword(s):  
Cell Wall ◽  
C4 Photosynthesis ◽  
Nile Red ◽  
Bundle Sheath ◽  
Setaria Viridis ◽  
Coding Region ◽  
Gene Coding ◽  
Suberin Lamellae ◽  
Type C ◽  
Gas Tight

AbstractC4 photosynthesis provides an effective solution for overcoming the catalytic inefficiency of Rubisco. The pathway is characterised by a biochemical CO2 concentrating mechanism that operates across mesophyll and bundle sheath (BS) cells and relies on a gas tight BS compartment. A screen of a mutant population of Setaria viridis, an NADP-malic enzyme type C4 monocot, generated using N-nitroso-N-methylurea identified a mutant with an amino acid change in the gene coding region of the ABCG transporter, a step in the suberin synthesis pathway. Here, Nile red staining, TEM, and GC/MS confirmed the alteration in suberin deposition in the BS cell wall of the mutant. We show that this has disrupted the suberin lamellae of BS cell wall and increased BS conductance to CO2 diffusion more than two-fold in the mutant. Consequently, BS CO2 partial pressure is reduced and CO2 assimilation was impaired in the mutant. Our findings provide experimental evidence that a functional suberin lamellae is an essential anatomical feature for efficient C4 photosynthesis in NADP-ME plants like S. viridis and have implications for engineering strategies to ensure future food security.

Functional compartmentation of C4 photosynthesis in the triple layered chlorenchyma of Aristida (Poaceae)

2005 ◽  
Vol 32 (1) ◽  
pp. 67 ◽  
Author(s):  
Elena V. Voznesenskaya ◽  
Simon D. X. Chuong ◽  
Nuria K. Koteyeva ◽  
Gerald E. Edwards ◽  
Vincent R. Franceschi
Keyword(s):  
Vascular Tissue ◽  
C4 Photosynthesis ◽  
Cell Types ◽  
Bundle Sheath ◽  
Mesophyll Cells ◽  
Western Blots ◽  
Kranz Anatomy ◽  
Bundle Sheath Cells ◽  
Low Levels ◽  
And Function

The genus Aristida (Poaceae), is composed of species that have Kranz anatomy and C4 photosynthesis. Kranz anatomy typically consists of two photosynthetic cell types: a layer of mesophyll cells where atmospheric CO2 is fixed into C4 acids, and an internal, chlorenchymatous vascular bundle sheath to which C4 acids are transferred and then decarboxylated to donate CO2 to the C3 cycle. The anatomy of Aristida species is unusual as it has three distinct layers of chlorenchyma cells surrounding the vascular tissue: an inner bundle sheath, an outer bundle sheath and the mesophyll cells. In this study of Aristida purpurea Nutt. var. longiseta, the functions of the three layers of chlorenchyma cells relative to the C4 photosynthetic mechanism were determined using ultrastructural analysis, western blots, immunolocalisation of photosynthetic enzymes and starch histochemistry. The results indicate that mesophyll cells contain high levels of phosphoenolpyruvate carboxylase (PEPC) and pyruvate Pi dikinase (PPDK), and function to capture CO2 in the C4 cycle. The inner bundle sheath, which is high in Rubisco and contains NADP-malic enzyme and glycine decarboxylase, functions to transfer CO2 to the C3 cycle through decarboxylation of C4 acids and by decarboxylation of glycine in the glycolate pathway. The outer chlorenchymatous sheath is where ADPG pyrophosphorylase is mainly located, and this cell layer functions as the primary site of starch storage. The outer sheath, which has low levels of Rubisco and PEPC, may also have a role in refixation of any CO2 that leaks from the inner bundle sheath cells.

scholarly journals Transcriptome and metabolome profiling provide insights into molecular mechanism of pseudostem elongation in banana

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Guiming Deng ◽  
Fangcheng Bi ◽  
Jing Liu ◽  
Weidi He ◽  
Chunyu Li ◽  
...  
Keyword(s):  
Cell Wall ◽  
Cell Elongation ◽  
Molecular Mechanisms ◽  
Specific Gene ◽  
Wild Type ◽  
Banana Plant ◽  
Cell Wall Modification ◽  
Dwarf Cultivar ◽  
Important Trait ◽  
Metabolome Profiling

AbstractBackgroundBanana plant height is an important trait for horticultural practices and semi-dwarf cultivars show better resistance to damages by wind and rain. However, the molecular mechanisms controlling the pseudostem height remain poorly understood. Herein, we studied the molecular changes in the pseudostem of a semi-dwarf banana mutant Aifen No. 1 (Musaspp. Pisang Awak sub-group ABB) as compared to its wild-type dwarf cultivar using a combined transcriptome and metabolome approach.ResultsA total of 127 differentially expressed genes and 48 differentially accumulated metabolites were detected between the mutant and its wild type. Metabolites belonging to amino acid and its derivatives, flavonoids, lignans, coumarins, organic acids, and phenolic acids were up-regulated in the mutant. The transcriptome analysis showed the differential regulation of genes related to the gibberellin pathway, auxin transport, cell elongation, and cell wall modification. Based on the regulation of gibberellin and associated pathway-related genes, we discussed the involvement of gibberellins in pseudostem elongation in the mutant banana. Genes and metabolites associated with cell wall were explored and their involvement in cell extension is discussed.ConclusionsThe results suggest that gibberellins and associated pathways are possibly developing the observed semi-dwarf pseudostem phenotype together with cell elongation and cell wall modification. The findings increase the understanding of the mechanisms underlying banana stem height and provide new clues for further dissection of specific gene functions.

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