Expression of the C4 Me1 Gene from Flaveria Bidentis Requires an Interaction Between 5[prime] and 3[prime] Sequences

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2002 Sep 19

PMID 12237394

Citations 22

Authors

J S Marshall

J D STUBBS

J. A. Chitty

B. Surin

W C Taylor

Affiliations

Soon will be listed here.

Abstract

The efficient functioning of C4 photosynthesis requires the strict compartmentation of a suite of enzymes in either mesophyll or bundle sheath cells. To determine the mechanism controlling bundle sheath cell-specific expression of the NADP-malic enzyme, we made a set of chimeric constructs using the 5[prime] and 3[prime] regions of the Flaveria bidentis Me1 gene fused to the [beta]-glucuronidase gusA reporter gene. The pattern of GUS activity in stably transformed F. bidentis plants was analyzed by histochemical and cell separation techniques. We conclude that the 5[prime] region of Me1 determines bundle sheath specificity, whereas the 3[prime] region contains an apparent enhancer-like element that confers high-level expression in leaves. The interaction of 5[prime] and 3[prime] sequences was dependent on factors that are present in the C4 plant but not found in tobacco.

Citing Articles

Agrobacterium-mediated transient transformation of Flaveria bidentis leaves: a novel method to examine the evolution of C photosynthesis.

Baros C, Beerkens J, Ludwig M Plant Methods. 2024; 20(1):193.

PMID: 39731143 PMC: 11674322. DOI: 10.1186/s13007-024-01306-z.

Plant terminators: the unsung heroes of gene expression.

de Felippes F, Waterhouse P J Exp Bot. 2022; 74(7):2239-2250.

PMID: 36477559 PMC: 10082929. DOI: 10.1093/jxb/erac467.

The evolution of C photosynthesis.

Sage R New Phytol. 2021; 161(2):341-370.

PMID: 33873498 DOI: 10.1111/j.1469-8137.2004.00974.x.

Plant 3' Regulatory Regions From mRNA-Encoding Genes and Their Uses to Modulate Expression.

Bernardes W, Menossi M Front Plant Sci. 2020; 11:1252.

PMID: 32922424 PMC: 7457121. DOI: 10.3389/fpls.2020.01252.

C3 cotyledons are followed by C4 leaves: intra-individual transcriptome analysis of Salsola soda (Chenopodiaceae).

Lauterbach M, Billakurthi K, Kadereit G, Ludwig M, Westhoff P, Gowik U J Exp Bot. 2016; 68(2):161-176.

PMID: 27660482 PMC: 5853821. DOI: 10.1093/jxb/erw343.

References

Matsuoka M, Kyozuka J, Shimamoto K, Kano-Murakami Y . The promoters of two carboxylases in a C4 plant (maize) direct cell-specific, light-regulated expression in a C3 plant (rice). Plant J. 1994; 6(3):311-9. DOI: 10.1046/j.1365-313x.1994.06030311.x. View

Sheen J . Metabolic repression of transcription in higher plants. Plant Cell. 1990; 2(10):1027-38. PMC: 159951. DOI: 10.1105/tpc.2.10.1027. View

Dean C, Favreau M, Bedbrook J, Dunsmuir P . Sequences downstream of translation start regulate quantitative expression of two petunia rbcS genes. Plant Cell. 1989; 1(2):201-8. PMC: 159752. DOI: 10.1105/tpc.1.2.201. View

Wang J, LONG J, Hotchkiss T, Berry J . C4 Photosynthetic Gene Expression in Light- and Dark-Grown Amaranth Cotyledons. Plant Physiol. 1993; 102(4):1085-1093. PMC: 158893. DOI: 10.1104/pp.102.4.1085. View

Matsuoka M, Numazawa T . Cis-acting elements in the pyruvate, orthophosphate dikinase gene from maize. Mol Gen Genet. 1991; 228(1-2):143-52. DOI: 10.1007/BF00282459. View

Purcell M, Mabrouk Y, Bogorad L . Red/far-red and blue light-responsive regions of maize rbcS-m3 are active in bundle sheath and mesophyll cells, respectively. Proc Natl Acad Sci U S A. 1995; 92(25):11504-8. PMC: 40430. DOI: 10.1073/pnas.92.25.11504. View

Stockhaus J, Schlue U, Koczor M, Chitty J, Taylor W, Westhoff P . The Promoter of the Gene Encoding the C4 Form of Phosphoenolpyruvate Carboxylase Directs Mesophyll-Specific Expression in Transgenic C4 Flaveria spp. Plant Cell. 1997; 9(4):479-489. PMC: 156933. DOI: 10.1105/tpc.9.4.479. View

Fu H, Kim S, Park W . High-level tuber expression and sucrose inducibility of a potato Sus4 sucrose synthase gene require 5' and 3' flanking sequences and the leader intron. Plant Cell. 1995; 7(9):1387-94. PMC: 160959. DOI: 10.1105/tpc.7.9.1387. View

Fu H, Kim S, Park W . A potato Sus3 sucrose synthase gene contains a context-dependent 3' element and a leader intron with both positive and negative tissue-specific effects. Plant Cell. 1995; 7(9):1395-403. PMC: 160961. DOI: 10.1105/tpc.7.9.1395. View

10.

Graham M, Larkin P . Adenine methylation at dam sites increases transient gene expression in plant cells. Transgenic Res. 1995; 4(5):324-31. DOI: 10.1007/BF01972529. View

11.

Marshall J, STUBBS J, Taylor W . Two genes encode highly similar chloroplastic NADP-malic enzymes in Flaveria. Implications for the evolution of C4 photosynthesis. Plant Physiol. 1996; 111(4):1251-61. PMC: 161004. DOI: 10.1104/pp.111.4.1251. View

12.

Stockhaus J, Poetsch W, Steinmuller K, Westhoff P . Evolution of the C4 phosphoenolpyruvate carboxylase promoter of the C4 dicot Flaveria trinervia: an expression analysis in the C3 plant tobacco. Mol Gen Genet. 1994; 245(3):286-93. DOI: 10.1007/BF00290108. View

13.

Furbank R, Taylor W . Regulation of Photosynthesis in C3 and C4 Plants: A Molecular Approach. Plant Cell. 1995; 7(7):797-807. PMC: 160868. DOI: 10.1105/tpc.7.7.797. View

14.

Matsuoka M, Sanada Y . Expression of photosynthetic genes from the C4 plant, maize, in tobacco. Mol Gen Genet. 1991; 225(3):411-9. DOI: 10.1007/BF00261681. View

15.

Dietrich R, Radke S, Harada J . Downstream DNA sequences are required to activate a gene expressed in the root cortex of embryos and seedlings. Plant Cell. 1992; 4(11):1371-82. PMC: 160225. DOI: 10.1105/tpc.4.11.1371. View

16.

Peleman J, Boerjan W, Engler G, Seurinck J, Botterman J, Alliotte T . Strong cellular preference in the expression of a housekeeping gene of Arabidopsis thaliana encoding S-adenosylmethionine synthetase. Plant Cell. 1989; 1(1):81-93. PMC: 159739. DOI: 10.1105/tpc.1.1.81. View

17.

Thornburg R, An G, Cleveland T, Johnson R, Ryan C . Wound-inducible expression of a potato inhibitor II-chloramphenicol acetyltransferase gene fusion in transgenic tobacco plants. Proc Natl Acad Sci U S A. 1987; 84(3):744-8. PMC: 304292. DOI: 10.1073/pnas.84.3.744. View

18.

Boinski J, Wang J, Xu P, Hotchkiss T, Berry J . Post-transcriptional control of cell type-specific gene expression in bundle sheath and mesophyll chloroplasts of Amaranthus hypochondriacus. Plant Mol Biol. 1993; 22(3):397-410. DOI: 10.1007/BF00015971. View

19.

Matsuoka M, Tada Y, Fujimura T, Kano-Murakami Y . Tissue-specific light-regulated expression directed by the promoter of a C4 gene, maize pyruvate,orthophosphate dikinase, in a C3 plant, rice. Proc Natl Acad Sci U S A. 1993; 90(20):9586-90. PMC: 47614. DOI: 10.1073/pnas.90.20.9586. View

20.

Sheen J . Molecular mechanisms underlying the differential expression of maize pyruvate, orthophosphate dikinase genes. Plant Cell. 1991; 3(3):225-45. PMC: 159995. DOI: 10.1105/tpc.3.3.225. View