Transcription control of the 32 kDa-QB protein of photosystem II in differentiated bundle sheath and mesophyll chloroplasts of maize (original) (raw)
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Current Genetics, 2011
The C4 grass Zea mays separates light and light-independent photosynthetic processes into two leaf cell types: bundle sheath (BS) and mesophyll (M). When mature, BS and M cells have anatomically and biochemically distinct chloroplasts that must cooperate to complete the process of photosynthesis. This report compares changes in transcript abundance between young and mature maize BS and M chloroplasts from speciWc segments of the leaf developmental gradient. Representative transcripts encoding components of Photosystem I, Photosystem II, Cytochrome b 6 f, thylakoidal NADH dehydrogenase; and the large subunit of ribulose-1,5-bisphosphate carboxylase/ oxygenase as well as nine nuclear-coded transcripts encoding chloroplast proteins were measured using quantitative RT-PCR. In addition, 887 nuclear genes encoding plastidlocalized proteins, as well as 64 chloroplast and 34 mitochondrial genes were assayed utilizing a cDNA microarray. In 9 out of the 18 chloroplast-encoded genes and 84 genes from the 985 element microarray revealed greater than twofold transcript abundance diVerences between developmental stages and/or cell types. Patterns for transcripts associated with operons and gene clusters suggest diVering regulatory mechanisms for particular polycistronic stretches. In summary, this report provides evidence that cell type-speciWc transcript abundance varies more in the young developing chloroplast, and diVerences plateau or subside as chloroplasts mature.
Plant and Cell Physiology, 2000
To characterize novel genes functioning specifically in mesophyll cells (MCs) or bundle sheath cells (BSCs) of C4 plants, differential screening of a maize cDNA library was conducted using 32 P-labeled single-strand cDNAs prepared from MCs and bundle sheath strands (BSS) as probes. Ten genes encoding thylakoid membrane proteins in chloroplasts were identified as MC-abundant genes. These included genes for chlorophyll a/b binding proteins, plastocyanin, PsaD, PsbT, PsbR, PsbO, PsaK, PsaG, PsaN and ferredoxin. Seven genes identified as BSS-abundant genes encoded PEP carboxykinase, salt-inducible SalT homolog, heavy metalinducible metallothionein-like protein, ABA-and droughtinducible glycine-rich protein, and three proteins of unknown function (one of which was named Bss1). In situ hybridization analyses for several selected genes revealed that mRNAs for the metallothionein-like protein and Bss1 were accumulated specifically in BSCs, and that mRNA for the SalT homolog was accumulated in vascular cells around phloem cells. Results suggest that the functional differentiation of MC chloroplasts accompany preferential expression of these small proteins in photosystem complexes and that BSCs are the major site of stress responses.
Biochimica et Biophysica Acta (BBA) - Bioenergetics, 2009
Photoinhibition is caused by an imbalance between the rates of the damage and repair cycle of photosystem II D1 protein in thylakoid membranes. The PSII repair processes include (i) disassembly of damaged PSII-LHCII supercomplexes and PSII core dimers into monomers, (ii) migration of the PSII monomers to the stroma regions of thylakoid membranes, (iii) dephosphorylation of the CP43, D1 and D2 subunits, (iv) degradation of damaged D1 protein, and (v) co-translational insertion of the newly synthesized D1 polypeptide and reassembly of functional PSII complex. Here, we studied the D1 turnover cycle in maize mesophyll and bundle sheath chloroplasts using a protein synthesis inhibitor, lincomycin. In both types of maize chloroplasts, PSII was found as the PSII-LHCII supercomplex, dimer and monomer. The PSII core and the LHCII proteins were phosphorylated in both types of chloroplasts in a light-dependent manner. The rate constants for photoinhibition measured for lincomycin-treated leaves were comparable to those reported for C3 plants, suggesting that the kinetics of the PSII photodamage is similar in C3 and C4 species. During the photoinhibitory treatment the D1 protein was dephosphorylated in both types of chloroplasts but it was rapidly degraded only in the bundle sheath chloroplasts. In mesophyll chloroplasts, PSII monomers accumulated and little degradation of D1 protein was observed. We postulate that the low content of the Deg1 enzyme observed in mesophyll chloroplasts isolated from moderate light grown maize may retard the D1 repair processes in this type of plastids.
Differential expression of LHCII genes in mesophyll and bundle sheath cells of maize
Carlsberg Research Communications, 1986
The properties and composition of bundle sheath and mesophyl! thylakoids from maize leaves are compared. This was possible because of the isolation of large amounts of purified material obtained by enzymatic digestion of mechanically disrupted leaves. Bundle sheath thylakoids from mature leaves, lack the chlorophyll-proteins and polypeptides associated with the reaction centre ofphotosystem II. They do, however, contain significant amounts of LHCII, which transfers excitation energy to photosystem I. LHCII isolated from bundle sheath thylakoids had a different freeze-fracture ultrastructure and a different polypeptide composition from LHCII isolated from mesophyll thylakoids, indicating a differential expression of the LHCII gene family in mesophyll and bundle sheath cells of maize leaves.
Transcriptional activity of isolated maize chloroplasts
Archives of Biochemistry and Biophysics, 1984
Chloroplasts and etioplasts, isolated from light-or dark-grown Zea mays plants, respectively, can incorporate labeled UTP into RNA in a reaction stimulated by light or ATP. This in organello RNA synthesis proceeded at a linear rate for up to 2 h. When expressed per unit protein, plastids from dark-grown plants incorporated more UTP than those from light-grown plants, and the highest rate of UTP incorporation was found in plastids from light-stimulated leaves (grown previously in the dark). The in organello newly synthesized RNA was heterodispersed, with most transcripts smaller than 14 S. Specific transcripts were detected in organelles from both darkand light-grown plants that contain sequences that are homologous to the mRNAs for the rbcL gene (coding for the large subunit of ribulose bisphosphate carboxylase (LS-RuBPCase)) and for the psbA gene (32-kDa thylakoid membrane protein). Qualitatively, the newly synthesized in wrganello transcripts were similar from the dark _-and light organelles. Q 1984 Academic PRSS. IN.
Plant Physiology, 1990
Phytochrome and the blue ultraviolet-A photoreceptor control light-induced expression of genes encoding the chlorophyll a/b binding protein of photosystem 11 and photosystem I and the genes for the small subunit of the ribulose-1,5-bisphosphate carboxylase in etiolated seedlings of Lycopersicon esculentum (tomato) and Nicotiana tabacum (tobacco). A 'high irradiance response' also controls the induction of these genes. Gernes encoding photosystem 11-and I-associated chlorophyll a/b binding proteins both exhibit a transient rapid increase in expression in response to light pulse or to continuous irradiation. In contrast, genes encoding the small subunit exhibit a continuous increase in expression in response to light. These distinct expression characteristics are shown to reflect differences at the level of transcription. Higher plants have several photoreceptors which detect light quality and intensity. The major photoreceptors are phytochrome (26), which control induction and 'high irradiance responses' (HIR2) (10), a blue/UV-A photoreceptor (27), and a UV-B photoreceptor (34). Studies of expression of nuclear genes encoding CAB, SSU, and CHS proteins revealed that photoregulation of gene expression in higher plants occurs at transcriptional and posttranscriptional levels (33). The dependence ofgene expression on light quality and intensity varies for different genes and different species. For instance, in parsley cell suspension cultures excitation of the UV-B photoreceptor is essential for maximal expression of CHS, while the excitation of the blue/
Organization and activity of photosystems in the mesophyll and bundle sheath chloroplasts of maize
Journal of Plant Physiology, 2006
Photosystem I and Photosystem II activities, as well as polypeptide content of chlorophyll (Chl)-protein complexes were analyzed in mesophyll (M) and bundle sheath (BS) chloroplasts of maize (Zea mays L.) growing under moderate and very low irradiance. This paper discusses the application of two techniques: mechanical and enzymatic, for separation of M and BS chloroplasts. The enzymatic isolation method resulted in depletion of polypeptides of oxygen evolving complex (OEC) and aCF1 subunit of coupling factor; D1 and D2 polypeptides of PSII were reduced by 50%, whereas light harvesting complex of photosystem II (LHCII) proteins were still detectable. Loss of PSII polypeptides correlated with the decreasing of Chl fluorescence measured at room temperature. Using mechanical isolation of chloroplasts from BS cells, all tested polypeptides could be detected. We found a total lack of O 2 evolution in BS chloroplasts, but dichlorophenolindophenol (DCPIP) was photoreduced. PSI activity of chloroplasts isolated from 14-and 28-day-old plants was similar in BS chloroplasts in moderate light (ML), but in low light (LL) it was reduced by about 20%. PSI and PSII activities in M chloroplasts of plants growing in ML decreased with aging of plants. In older LL-grown plants, activities of both photosystems were higher than those observed in chloroplasts from ML-grown plants.
Journal of Plant Physiology, 2003
Norflurazon, an inhibitor of carotenoid synthesis, is known to cause photooxidative destruction of chloroplasts. Expression of many nuclear genes for chloroplast-destined proteins is suppressed in the photobleached seedlings due to impairment of signaling from chloroplasts to nuclei. Here the effect of norflurazon-treatment on the expression of genes for C4 photosynthesis was investigated. Unlike the genes of Cab and RbcS, the levels of mRNA for pyruvate Pi dikinase and NADP-malic enzyme were not markedly reduced. However, their protein levels were more significantly reduced suggesting a control by chloroplast exerted at the translational step. From their molecular sizes these proteins seemed to have been correctly processed and hence localized in the rudimental chloroplasts. In support of this, 9 kinds of proteins for chloroplast biogenesis such as Toc family and Hsp70 proteins were not suppressed, suggesting that protein import machinery and processing are still functional in the cells harboring rudimental chloroplasts. Diurnal changes of the levels of transcripts for photosynthetic genes persisted in the norflurazon-treated seedlings indicating non-involvement of chloroplast in this light control.
Proceedings of the National Academy of Sciences, 1992
Cell-specific and light-regulated expression of the beta-glucuronidase (GUS) reporter gene from maize cab-m1 and rbcS-m3 promoter sequences was studied in maize leaf segments by using an in situ transient expression microprojectile bombardment assay. The cab-m1 gene is known to be strongly photoregulated and to be expressed almost exclusively in mesophyll cells (MC) but not in bundle sheath cells (BSC). Expression of GUS from a 1026-base-pair 5' promoter fragment of cab-m1 is very low in dark-grown leaves; GUS expression is increased about 10-fold upon illumination of dark-grown leaves. In illuminated leaves, the ratio of GUS expression in MC vs. BSC is about 10:1. The cab-m1 region between 868 and 1026 base pairs 5' to the translation start confers strong MC-preferred expression on the remainder of the chimeric gene in illuminated leaves, but a region between -39 and -359 from the translation start is required for photoregulated expression. Transcripts of rbcS-m3 are found ...
The Plant Cell, 1996
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-mutablel (bsd2-ml) 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.