Differential Expression Pattern of C4 Bundle Sheath Expression Genes in Rice, a C3 Plant

Nomura, Masatoshi; Higuchi, Tomonori; Ishida, Yuji; Ohta, Shozo; Komari, Toshihiko; Imaizumi, Nobuyuki; Miyao-Tokutomi, Mitsue; Matsuoka, Makoto; Tajima, Shigeyuki

doi:10.1093/pcp/pci078

Cited by 56 publications

(44 citation statements)

References 33 publications

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“…The special physiology of bundle-sheath cells in Arabidopsis and the fact that preexisting transcription factors in this C 3 species are able to recognize heterologous C 4 -characteristic cis-regulatory elements in the correct fashion provide further evidence for the view that the evolution of C 4 plants must have been relatively simple in genetic terms . C 4 -like spatial activities of C 4 promoters in transgenic C 3 plants have also been reported for the C 4 isoform of PEPC of maize (Zea mays; Matsuoka et al, 1994;Nomura et al, 2000), the pyruvate orthophosphate dikinase gene of maize (Matsuoka et al, 1993), and the phosphoenolpyruvate carboxykinase of Zoysia japonica (Nomura et al, 2005). On the other hand, the C 4 -PEPC promoter of F. trinervia loses mesophyll specificity when it is introduced in Arabidopsis (Akyildiz et al, 2007).…”

Section: Discussionmentioning

confidence: 87%

The Gene for the P-Subunit of Glycine Decarboxylase from the C4 SpeciesFlaveria trinervia: Analysis of Transcriptional Control in TransgenicFlaveria bidentis(C4) and Arabidopsis (C3)

et al. 2008

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Glycine decarboxylase (GDC) plays an important role in the photorespiratory metabolism of plants. GDC is composed of four subunits (P, H, L, and T) with the P-subunit (GLDP) serving as the actual decarboxylating unit. In C3 plants, GDC can be found in all photosynthetic cells, whereas in leaves of C3-C4 intermediate and C4 species its occurrence is restricted to bundle-sheath cells. The specific expression of GLDP in bundle-sheath cells might have constituted a biochemical starting point for the evolution of C4 photosynthesis. To understand the molecular mechanisms responsible for restricting GLDP expression to bundle-sheath cells, we performed a functional analysis of the GLDPA promoter from the C4 species Flaveria trinervia. Expression of a promoter-reporter gene fusion in transgenic plants of the transformable C4 species Flaveria bidentis (C4) showed that 1,571 bp of the GLDPA 5′ flanking region contain all the necessary information for the specific expression in bundle-sheath cells and vascular bundles. Interestingly, we found that the GLDPA promoter of F. trinervia exhibits a C4-like spatial activity also in the C3 plant Arabidopsis (Arabidopsis thaliana), indicating that a mechanism for bundle-sheath-specific expression is also present in this C3 species. Using transgenic Arabidopsis, promoter deletion studies identified two regions in the GLDPA promoter, one conferring repression of gene expression in mesophyll cells and one functioning as a general transcriptional enhancer. Subsequent analyses in transgenic F. bidentis confirmed that these two segments fulfill the same function also in the C4 context.

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Section: Discussionmentioning

confidence: 87%

The Gene for the P-Subunit of Glycine Decarboxylase from the C4 SpeciesFlaveria trinervia: Analysis of Transcriptional Control in TransgenicFlaveria bidentis(C4) and Arabidopsis (C3)

et al. 2008

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“…Although ZmSHR1 accumulates preferentially in bundle sheath cells of maize leaves (Tausta et al, 2014), the spatial domain of ZmSHR1 pro activity in rice has not been determined, whereas ZjPCK pro has been shown previously to direct gene expression in veins and mature bundle sheath cells of rice leaves and in the vasculature of rice roots (Nomura et al, 2005). Transgenic lines were recovered from transformations with three different constructs (ZmSHR1 pro :ZmSHR1, a translational reporter fusion [ZmSHR1 pro :mTurquoise::ZmSHR1], and ZjPCK pro :ZmSHR1).…”

Section: Ectopic Expression Of Zmshr1 Leads To the Formation Of Extramentioning

confidence: 99%

“…S1), demonstrating that ectopic SHR activity is sufficient to perturb stomatal patterning in the rice epidermis. Due to very low fertility in ZmSHR1 pro : ZmSHR1 and ZmSHR1 pro :mTurquoise::ZmSHR1 lines and given the known fidelity of ZjPCK pro for bundle sheath preferential activity in rice (Nomura et al, 2005), the ZjPCK pro :ZmSHR1 line was advanced for further phenotypic analysis. Three T1 individuals (207_ 29 , 207_ 30 , and 207_ 31 ) were propagated into the T2 generation, and then homozygous T2 lines (207 _29H , 207 _30K , and 207 _31J ) that encompassed a range of transgene expression levels (from 27-to 100-fold above background in the shoot) were selected for all subsequent analyses.…”

Section: Ectopic Expression Of Zmshr1 Leads To the Formation Of Extramentioning

confidence: 99%

“…The amplified sequence was subcloned into the Gateway donor vector pDONR207 in a BP reaction. The resultant entry clones were sequenced, and the target sequences were then cloned in an LR reaction downstream of Zoysia japonica PCK pro (Nomura et al, 2005) into a destination vector modified from pVec8-GFP (Kim and Dolan, 2016) or into the binary destination vector pSC210. pSC210 vector was created by Sarah Covshoff and kindly gifted to us by Julian Hibberd (University of Cambridge).…”

Section: Generation Of Transformation Constructsmentioning

confidence: 99%

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SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

et al. 2017

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ORCID IDs: 0000-0003-4287-6927 (M.L.S.); 0000-0002-7609-0378 (O.V.S.); 0000-0001-5932-6468 (B.J.W.); 0000-0002-4621-1490 (P.W.); 0000-0001-7648-3924 (J.A.L.).The coordinated positioning of veins, mesophyll cells, and stomata across a leaf is crucial for efficient gas exchange and transpiration and, therefore, for overall function. In monocot leaves, stomatal cell files are positioned at the flanks of underlying longitudinal leaf veins, rather than directly above or below. This pattern suggests either that stomatal formation is inhibited in epidermal cells directly in contact with the vein or that specification is induced in cell files beyond the vein. The SHORTROOT pathway specifies distinct cell types around the vasculature in subepidermal layers of both root and shoots, with cell type identity determined by distance from the vein. To test whether the pathway has the potential to similarly pattern epidermal cell types, we expanded the expression domain of the rice (Oryza sativa ssp japonica) OsSHR2 gene, which we show is restricted to developing leaf veins, to include bundle sheath cells encircling the vein. In transgenic lines, which were generated using the orthologous ZmSHR1 gene to avoid potential silencing of OsSHR2, stomatal cell files were observed both in the normal position and in more distant positions from the vein. Contrary to theoretical predictions, and to phenotypes observed in eudicot leaves, the increase in stomatal density did not enhance photosynthetic capacity or increase mesophyll cell density. Collectively, these results suggest that the SHORTROOT pathway may coordinate the positioning of veins and stomata in monocot leaves and that distinct mechanisms may operate in monocot and eudicot leaves to coordinate stomatal patterning with the development of underlying mesophyll cells.The coordinated differentiation of cell types within an organ is a crucial component of morphogenesis, necessary to ensure that the final form is appropriate for function. In this regard, photosynthetic function in plant leaves requires that chloroplast-containing cells in the middle leaf layers are interspersed with veins (to supply water and to redistribute metabolites) and are overlaid with stomatal pores through which carbon dioxide can enter the leaf. In grass leaves, cellular arrangements are defined by parallel longitudinal veins that extend from the base of the leaf sheath to the tip of the leaf blade, with short transverse veins interconnecting the longitudinal network (Sharman, 1942;Esau, 1943;Nelson and Dengler, 1997). This vascular framework underpins linear files of stomata in the epidermis, with each vein being flanked by one to three rows of stomata on both the medial and lateral sides (Stebbins and Shah, 1960). The genetic mechanisms that ensure optimal photosynthetic capacity in grass leaves, by coordinating the development of veins, photosynthetic cell types, and stomata, are not known.Grass leaves develop basipetally such that cellular differentiation proceeds from the tip of the leaf to the base, ...

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“…Transcripts detected with maize-specific ZmCA2 (2.0 kb), ZmDCT2 (1.9 kb), ZmMDH6 (1.5 kb), ZmDCT1 (2.1 kb), ZmME1 (2.2 kb), ZmPPDK (3.5 kb), ZmPEPC1 (3.2 kb), and ZmOMT1 (1.9 kb) probes were of the expected sizes. maize NADP-ME rice, in which the promoter of the maize NADP-ME gene was able to generate expression of the uidA reporter in rice (Nomura et al, 2005). The difference between the behavior of the maize NADP-ME gene in these C 3 crops is interesting and could be due to differences in transacting factors or, alternatively, to large-scale silencing of maize genes in the OMA lines.…”

Section: Several Maize Transcripts Associated With C 4 Photosynthesismentioning

confidence: 99%

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

et al. 2012

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C4 photosynthesis has evolved in at least 66 lineages within the angiosperms and involves alterations to the biochemistry, cell biology, and development of leaves. The characteristic “Kranz” anatomy of most C4 leaves was discovered in the 1890s, but the genetic basis of these traits remains poorly defined. Oat × maize addition lines allow the effects of individual maize (Zea mays; C4) chromosomes to be investigated in an oat (Avena sativa; C3) genetic background. Here, we have determined the extent to which maize chromosomes can introduce C4 characteristics into oat and have associated any C4-like changes with specific maize chromosomes. While there is no indication of a simultaneous change to C4 biochemistry, leaf anatomy, and ultrastructure in any of the oat × maize addition lines, the C3 oat leaf can be modified at multiple levels. Maize genes encoding phosphoenolpyruvate carboxylase, pyruvate, orthophosphate dikinase, and the 2′-oxoglutarate/malate transporter are expressed in oat and generate transcripts of the correct size. Three maize chromosomes independently cause increases in vein density, and maize chromosome 3 results in larger bundle sheath cells with increased cell wall lipid deposition in oat leaves. These data provide proof of principle that aspects of C4 biology could be integrated into leaves of C3 crops.

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Differential Expression Pattern of C4 Bundle Sheath Expression Genes in Rice, a C3 Plant

Cited by 56 publications

References 33 publications

The Gene for the P-Subunit of Glycine Decarboxylase from the C4 SpeciesFlaveria trinervia: Analysis of Transcriptional Control in TransgenicFlaveria bidentis(C4) and Arabidopsis (C3)

The Gene for the P-Subunit of Glycine Decarboxylase from the C4 SpeciesFlaveria trinervia: Analysis of Transcriptional Control in TransgenicFlaveria bidentis(C4) and Arabidopsis (C3)

SHORTROOT-Mediated Increase in Stomatal Density Has No Impact on Photosynthetic Efficiency

Individual Maize Chromosomes in the C3 Plant Oat Can Increase Bundle Sheath Cell Size and Vein Density

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