Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize.

Langdale, Jane A.; Zelitch, Israel; Miller, Edward J.; Nelson, Timothy

doi:10.1002/j.1460-2075.1988.tb03245.x

Cited by 167 publications

(150 citation statements)

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“…In contrast to amaranth, light appears to be a major signal that influences C4-type gene expression in the C4 monocot maize (Sheen and Bogarad, 1985;Langdale et al, 1988b;Langdale and Nelson, 1991). In dark-grown (etiolated) maize seedlings, RuBPCase mRNAs and proteins are found in both bundle sheath and mesophyll cells in a C3-like pattern.…”

Section: Discussionmentioning

confidence: 99%

“…In the C4 monocot maize, both cell position and light influence the bundle sheath cell-specific expression of RuBPCase genes (Sheen andBogarad, 1985, 1986;Langdale et al, 1988aLangdale et al, , 1988bNelson and Langdale, 1989). Recently, we reported that in the C4 dicot amaranth, the developmental stage of the leaf, rather than light, appears to control bundle sheath cell-specific expression of the RuBPCase LSU and SSU genes (Wang et al, 1992).…”

Section: Introductionmentioning

confidence: 99%

“…state (Langdale et al, 1988b;Langdale and Nelson, 1991;Wang et al, 1992). Specific signals are then required to suppress the expression of RuBPCase genes in mesophyll cells while allowing their continued expression in bundle sheath cells.…”

Section: Introductionmentioning

confidence: 99%

“…In very young (5-mm-long) amaranth leaves, the RuBPCase genes were expressed in a pattern similar to that observed in plants that use the C3 photosynthetic pathway, with LSU and SSU proteins and mRNAs present in both bundle sheath and mesophyll cells. The RuBPCase proteins and mRNAs became specifically localized to bundle sheath cells in the characteristic C4-type pattern as the leaves expanded to 10 mm in length over the time period of 24 to 36 hr.It is probable that C3-like expression of RuBPCase genes in both photosynthetic cell types represents an initial "default" Langdale et al, 1988b;Langdale and Nelson, 1991;Wang et al, 1992). Specific signals are then required to suppress the expression of RuBPCase genes in mesophyll cells while allowing their continued expression in bundle sheath cells.…”

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Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

et al. 1993

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Plants that use the highly efficient C4 photosynthetic pathway possess two types of specialized leaf cells, the mesophyll and bundle sheath. In mature C4 leaves, the C02 fixation enzyme ribulose-l,5-bisphosphate carboxylase (RuBPCase) is specifically compartmentalized to the bundle sheath cells. However, in very young leaves of amaranth, a dicotyledonous C4 plant, genes encoding the large subunit and small subunit of RuBPCase are initially expressed in both photosynthetic cell types. We show here that the RuBPCase mRNAs and proteins become specifically localized to leaf bundle sheath cells during the developmental transition of the leaf from carbon sink to carbon source. Bundle sheath cell-specific expression of RuBPCase genes and the sink-to-source transition began initially at the leaf apex and progressed rapidly and coordinately toward the leaf base. These findings demonstrated that two developmental transitions, the change in photoassimilate transport status and the establishment of bundle sheath cell-specific RuBPCase gene expression, are tightly coordinated during C4 leaf development. This correlation suggests that processes associated with the accumulation and transport of photosynthetic compounds may influence patterns of photosynthetic gene expression in C4 plants. INTRODUCTIONRibulose-1 5bisphosphate carboxylase (RuBPCase) is located in the chloroplasts of all higher plants and is the principal enzyme in photosynthetic carbon fixation. This enzyme is composed of two subunits, the chloroplast-encoded large subunit (LSU) and the nuclear-encoded small subunit (SSU) (Ellis, 1981; Miziorko and Lorimer, 1983). In plant species that utilize the C3 photosynthetic pathway, RuBPCase is found in all of the photosynthetic cells of the leaf. In mature leaves of plants that utilize the more complex C4 photosynthetic pathway, RuBPCase is specifically localized to one specialized cell type, the bundle sheath cells (Hatch and Slack, 1970;Edwards and Huber, 1981). Bundle sheath cells in C4 leaves occur as one or two rings around each of the leaf veins. Mesophyll cells, the other photosynthetic cell type in C4 plants, surround each ring of bundle sheath cells in one or more layers.The two types of photosynthetic cells compartmentalize the different reactions of the C4 pathway (Hatch and Slack, 1970;Gutierrez et al., 1974;Edwards and Huber, 1981). In C4 plants, the initial fixation of atmospheric COe is accomplished by the enzyme phosphoenolpyruvate carboxylase, which is found only in mesophyll cells. The carboxylation phase of the C4 pathway in mesophyll cells produces C4 acids, which are then transported to neighboring bundle sheath cells. In bundle sheath cells, decarboxylation of the C4 acids releases COn To whom correspondence should be addressed.for refixation by RuBPCase. These reactions cause COn to be concentrated in bundle sheath cells in the vicinity of RuBPCase, thereby increasing photosynthetic efficiency and reducing metabolically wasteful photorespiration caused by the oxygenase activity of this enzyme.The ...

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

mentioning

confidence: 99%

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Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

et al. 1993

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“…There was no evidence that the proximity of the vascular tissue influenced development of photochemical function as in corn (9). Imaging of the tip of a young cucumber leaf on consecutive days showed homogeneity in kinetics in the interveinal areas with similar changes occurring at all points on a day to day basis (Fig.…”

mentioning

confidence: 93%

Patterns of Chlorophyll Fluorescence Kinetics in Relation to Growth and Expansion in Cucumber Leaves

Croxdale¹,

Omasa²

1990

Plant Physiol.

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MATERIALS AND METHODSPhotochemical development was studied in developing cucumber (Cucumis sativus L. cv Hokushin) leaves to determine if the spatial pattern coincided with relative growth rates of expanding leaves, intercalary cell division, or position relative to the vascular tissue. Both leaf surfaces undergo a series of similar changes in chlorophyll a fluorescence kinetics, but the upper surface more quickly achieved the characteristic response. Imaging of fluorescence showed an individual developing leaf has four regions differing in kinetics, but these regions do not coincide with areas of increasing relative growth rate. Two of these regions lie at the leaf edge and their divergent kinetics may be related to structural and physiological features present at this position. A third area with different kinetics, in the basal region of the leaf, is spatially consistent with primordial regions that are clonal during development. The correspondence between areas of clonal growth and specific fluorescence kinetics indicates that cells of common ancestry show functional uniformity. No evidence was found that the proximity of the vascular tissue influenced development of photochemical function.The attainment of photosynthetic competency in angiosperm leaves is regulated by light and by developmental factors. Unlike monocots such as wheat (2), cucumber leaves are not photochemically competent when first exposed to light, but acquire competency over an extended time period, 6 d or more in the light (5). Within these leaves photochemical activity is not homogeneous, but develops basipetally as shown by Chl a fluorescence transients. These data indicate that the primary regulation ofthe development ofphotochemical activity lies with developmental factors, not light (5).Although the attainment of characteristic fluorescence transients progresses in a basipetal direction, mirroring the general direction ofexpansion and growth ofthe leaf(5), the influence of developmental factors from cells and tissues within the leaves has not been studied. The objective of the present research was to determine ifthe spatial pattern of photochemical development coincided with leaf expansion and relative growth rates, intercalary cell division, or position relative to the vascular tissue. With the availability of dynamic imaging of Chl a fluorescence (10), a precise, nondestructive means of studying these influences exists.'Supported by a National Science Foundation grant (JGC). Plant Materials and Leaf Area MeasurementsCucumber (Cucumis sativus L. cv Hokushin) plants were grown as previously described (10) for up to 5 weeks. For fluorescence and gas exchange measurements, plants were brought from the controlled-environment greenhouse to the laboratory and allowed to acclimate for about 2 h. Plants were dark-incubated for at least 30 min before fluorescence induction. No appreciable differences in induction kinetics were observed with longer dark periods. Leaves monitored for fluorescence and assimilation were intact and remain...

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TheKnottedleaf blade is a mosaic of blade, sheath, and auricle identities

Sinha

Hake

1994

Dev. Genet.

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Cell position and light influence C4 versus C3 patterns of photosynthetic gene expression in maize.

Cited by 167 publications

References 17 publications

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

Carbon Sink-to-Source Transition Is Coordinated with Establishment of Cell-Specific Gene Expression in a C4 Plant.

Patterns of Chlorophyll Fluorescence Kinetics in Relation to Growth and Expansion in Cucumber Leaves

TheKnottedleaf blade is a mosaic of blade, sheath, and auricle identities

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