Abstract
Within the maize leaf primordium, coordinated cell division and differentiation patterns result in the development of two morphologically and biochemically distinct photosynthetic cell types, the bundle sheath and the mesophyll. The bundle sheath defective2-mutable1 (bsd2-m1) mutation specifically disrupts C4 differentiation in bundle sheath cells in that the levels of bundle sheath cell-specific photosynthetic enzymes are reduced and the bundle sheath chloroplast structure is aberrant. In contrast, mesophyll cell-specific enzymes accumulate to normal levels, and the mesophyll cell chloroplast structure is not perturbed. Throughout mutant leaf development, the large and small subunits of ribulose bisphosphate carboxylase are absent; however, both rbcL and RbcS transcripts accumulate. Moreover, chloroplast-encoded rbcL transcripts accumulate ectopically in mesophyll cells. Although the bundle sheath cell chloroplast structure deteriorates rapidly when plants are exposed to light, this deterioration is most likely a secondary effect resulting from cell-specific photooxidative damage. Therefore, we propose that the Bsd2 gene plays a direct role in the post-transcriptional control of rbcL transcript accumulation and/or translation, both in bundle sheath and mesophyll cells, and an indirect role in the maintenance of bundle sheath cell chloroplast structure.
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- Allen R. D. Dissection of Oxidative Stress Tolerance Using Transgenic Plants. Plant Physiol. 1995 Apr;107(4):1049–1054. doi: 10.1104/pp.107.4.1049. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Avni A., Edelman M., Rachailovich I., Aviv D., Fluhr R. A point mutation in the gene for the large subunit of ribulose 1,5-bisphosphate carboxylase/oxygenase affects holoenzyme assembly in Nicotiana tabacum. EMBO J. 1989 Jul;8(7):1915–1918. doi: 10.1002/j.1460-2075.1989.tb03594.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bansal K. C., Viret J. F., Haley J., Khan B. M., Schantz R., Bogorad L. Transient expression from cab-m1 and rbcS-m3 promoter sequences is different in mesophyll and bundle sheath cells in maize leaves. Proc Natl Acad Sci U S A. 1992 Apr 15;89(8):3654–3658. doi: 10.1073/pnas.89.8.3654. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barkan A. Nuclear Mutants of Maize with Defects in Chloroplast Polysome Assembly Have Altered Chloroplast RNA Metabolism. Plant Cell. 1993 Apr;5(4):389–402. doi: 10.1105/tpc.5.4.389. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barkan A., Walker M., Nolasco M., Johnson D. A nuclear mutation in maize blocks the processing and translation of several chloroplast mRNAs and provides evidence for the differential translation of alternative mRNA forms. EMBO J. 1994 Jul 1;13(13):3170–3181. doi: 10.1002/j.1460-2075.1994.tb06616.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berry J. O., Nikolau B. J., Carr J. P., Klessig D. F. Transcriptional and post-transcriptional regulation of ribulose 1,5-bisphosphate carboxylase gene expression in light- and dark-grown amaranth cotyledons. Mol Cell Biol. 1985 Sep;5(9):2238–2246. doi: 10.1128/mcb.5.9.2238. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Boinski J. J., Wang J. L., Xu P., Hotchkiss T., Berry J. O. Post-transcriptional control of cell type-specific gene expression in bundle sheath and mesophyll chloroplasts of Amaranthus hypochondriacus. Plant Mol Biol. 1993 Jun;22(3):397–410. doi: 10.1007/BF00015971. [DOI] [PubMed] [Google Scholar]
- Camp P. J., Huber S. C., Burke J. J., Moreland D. E. Biochemical Changes that Occur during Senescence of Wheat Leaves : I. Basis for the Reduction of Photosynthesis. Plant Physiol. 1982 Dec;70(6):1641–1646. doi: 10.1104/pp.70.6.1641. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Danon A., Mayfield S. P. Light regulated translational activators: identification of chloroplast gene specific mRNA binding proteins. EMBO J. 1991 Dec;10(13):3993–4001. doi: 10.1002/j.1460-2075.1991.tb04974.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ford D. M., Shibles R. Photosynthesis and Other Traits in Relation to Chloroplast Number during Soybean Leaf Senescence. Plant Physiol. 1988 Jan;86(1):108–111. doi: 10.1104/pp.86.1.108. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Girard-Bascou J., Pierre Y., Drapier D. A nuclear mutation affects the synthesis of the chloroplast psbA gene production Chlamydomonas reinhardtii. Curr Genet. 1992 Jul;22(1):47–52. doi: 10.1007/BF00351741. [DOI] [PubMed] [Google Scholar]
- Goldschmidt-Clermont M., Girard-Bascou J., Choquet Y., Rochaix J. D. Trans-splicing mutants of Chlamydomonas reinhardtii. Mol Gen Genet. 1990 Sep;223(3):417–425. doi: 10.1007/BF00264448. [DOI] [PubMed] [Google Scholar]
- Hatch M. D. Regulation of enzymes in C4 photosynthesis. Curr Top Cell Regul. 1978;14:1–27. [PubMed] [Google Scholar]
- Jiang C. Z., Rodermel S. R. Regulation of Photosynthesis during Leaf Development in RbcS Antisense DNA Mutants of Tobacco. Plant Physiol. 1995 Jan;107(1):215–224. doi: 10.1104/pp.107.1.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kubicki A., Steinmüller K., Westhoff P. Differential transcription of plastome-encoded genes in the mesophyll and bundle-sheath chloroplasts of the monocotyledonous NADP-malic enzyme-type C4 plants maize and Sorghum. Plant Mol Biol. 1994 Jul;25(4):669–679. doi: 10.1007/BF00029605. [DOI] [PubMed] [Google Scholar]
- Langdale J. A., Metzler M. C., Nelson T. The argentia mutation delays normal development of photosynthetic cell-types in Zea mays. Dev Biol. 1987 Jul;122(1):243–255. doi: 10.1016/0012-1606(87)90349-6. [DOI] [PubMed] [Google Scholar]
- Langdale J. A., Rothermel B. A., Nelson T. Cellular pattern of photosynthetic gene expression in developing maize leaves. Genes Dev. 1988 Jan;2(1):106–115. doi: 10.1101/gad.2.1.106. [DOI] [PubMed] [Google Scholar]
- Langdale J. A., Zelitch I., Miller E., Nelson T. Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize. EMBO J. 1988 Dec 1;7(12):3643–3651. doi: 10.1002/j.1460-2075.1988.tb03245.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rodermel S. R., Abbott M. S., Bogorad L. Nuclear-organelle interactions: nuclear antisense gene inhibits ribulose bisphosphate carboxylase enzyme levels in transformed tobacco plants. Cell. 1988 Nov 18;55(4):673–681. doi: 10.1016/0092-8674(88)90226-7. [DOI] [PubMed] [Google Scholar]
- Schuster G., Gruissem W. Chloroplast mRNA 3' end processing requires a nuclear-encoded RNA-binding protein. EMBO J. 1991 Jun;10(6):1493–1502. doi: 10.1002/j.1460-2075.1991.tb07669.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheen J. Y., Bogorad L. Differential expression of the ribulose bisphosphate carboxylase large subunit gene in bundle sheath and mesophyll cells of developing maize leaves is influenced by light. Plant Physiol. 1985 Dec;79(4):1072–1076. doi: 10.1104/pp.79.4.1072. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sheen J. Metabolic repression of transcription in higher plants. Plant Cell. 1990 Oct;2(10):1027–1038. doi: 10.1105/tpc.2.10.1027. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sieburth L. E., Berry-Lowe S., Schmidt G. W. Chloroplast RNA Stability in Chlamydomonas: Rapid Degradation of psbB and psbC Transcripts in Two Nuclear Mutants. Plant Cell. 1991 Feb;3(2):175–189. doi: 10.1105/tpc.3.2.175. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sylvester A. W., Cande W. Z., Freeling M. Division and differentiation during normal and liguleless-1 maize leaf development. Development. 1990 Nov;110(3):985–1000. doi: 10.1242/dev.110.3.985. [DOI] [PubMed] [Google Scholar]
- Viret J. F., Mabrouk Y., Bogorad L. Transcriptional photoregulation of cell-type-preferred expression of maize rbcS-m3: 3' and 5' sequences are involved. Proc Natl Acad Sci U S A. 1994 Aug 30;91(18):8577–8581. doi: 10.1073/pnas.91.18.8577. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wardley T. M., Bhalla P. L., Dalling M. J. Changes in the Number and Composition of Chloroplasts during Senescence of Mesophyll Cells of Attached and Detached Primary Leaves of Wheat (Triticum aestivum L.). Plant Physiol. 1984 Jun;75(2):421–424. doi: 10.1104/pp.75.2.421. [DOI] [PMC free article] [PubMed] [Google Scholar]