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Cellular Pattern of Photosynthetic Gene Expression in Developing Maize Leaves

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Cellular Pattern of Photosynthetic Gene Expression in Developing Maize Leaves Downloaded from genesdev.cshlp.org on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Cellular pattern of photosynthetic gene expression in developing maize leaves Jane A. Langdale, Beverly A. Rothermel, and Timothy Nelson Department of Biology, Yale University, New Haven, Connecticut 06511 USA Leaf development in C4 plants such as maize involves the differentiation of two photosynthetic cell types [bundle sheath (BS) and mesophyll (M)] to form Kranz-type leaf anatomy. This cellular dimorphism partitions photosynthetic activities so that each enzyme of the C4 pathway accumulates only in the appropriate cell type. We have exploited this property to study BS and M cell interactions in developing maize leaves. Our previous studies showed that C4 proteins appear concurrently with the appearance of Kranz anatomy. To look at earlier events in BS and M cell development we have used three of the corresponding C4 mRNAs as cell-specific markers. We have followed, in situ, the accumulation of malic enzyme (ME), phosphoenolpyruvate carboxylase (PEPCase), and ribulose bisphosphate carboxylase (RuBPCase) mRNAs in developing leaves of both normal and mutant argentia (ar) maize. We have isolated a partial cDNA clone for maize ME to examine ME mRNA expression. We show that throughout the development of light-grown seedlings, all three mRNAs accumulate in a cell-specific fashion in both normal and ar leaves. The pattern of C4 mRNA accumulation longitudinally along the veins, laterally across the leaf, and locally around individual veins reveals the spatial and temporal sequence of BS and M cell development. BS cell-specific mRNAs accumulate around developing veins before Kranz anatomy is evident morphologically. Our analysis of the ar mutant, in which C4 mRNA appearance is delayed relative to the appearance of Kranz anatomy, demonstrates first that BS and M cells develop in clusters across the leaf blade and second that BS cells surrounding any individual vein are activated asynchronously. We discuss our results in relation to models and mechanisms of BS and M cell development. [Key Words: Leaf development; C4 photosynthesis; maize; in situ hybridization] Received July 6, 1987; revised version accepted November 20, 1987. Leaf development in all vascular plants is initiated contact with the epidermis. Although the photosynthetic within the vegetative shoot meristem. In graminaceous BS and M cells arise from two separate cell lineages (pro- plants, subsequent cell divisions and elongation occur cambium and ground meristem, respectively) (Dengler primarily from a basal intercalary meristem producing a et al. 1985; M. Freeling, pers. comm.), when fully differ- gradient of cells along the leaf, with the youngest at the entiated they must interact to fix CO2 (for a review, see base and the oldest at the tip (Sharman 1942). Successive Edwards and Huber 1981). The C4 pathway requires ma- transverse sections of a leaf therefore provide synchron- late dehydrogenase (MDH), phosphoenolpyruvate car- ized populations of cells at different developmental boxylase (PEPCase), and pyruvate phosphate dikinase stages. This property has been utilized to study various (PPdK) activities in the M cells and malic enzyme {ME) aspects of leaf development in both C3 plants such as and ribulose bisphosphate carboxylase (RuBPCase) activ- barley (Viro and Kloppstech 1980), oats (Taylor and ities in the BS cells. These enzymes are synthesized cy- Mackender 1977), and wheat (Dean and Leech 1982; toplasmically in a cell-specific manner and subsequently Aoyagi and Bassham 1986a) and C4 plants such as maize subcompartmentalized such that MDH and PPdK are (Leese and Leech 1976; Baker and Leech 1977; Williams found in M cell chloroplasts, PEPCase in M cell cyto- and Kennedy 1978; Miranda et al. 1981; Martineau and plasm, and ME and RuBPCase in BS cell chloroplasts Taylor 1985; Aoyagi and Bassham 1986b). (Edwards and Huber 1979; Broglie et al. 1984). PPdK has In C4 plants photosynthetic development is more also been detected in BS cell chloroplasts, but its func- complex than in C3 plants due to chloroplastic and cel- tion in these cells is unknown (Aoyagi and Nakamoto lular dimorphism. Photosynthesis in C3 plants requires 1985). only one photosynthetic cell type, whereas C4 plants The enzymes associated with C4 metabolism have rely on Kranz-type leaf anatomy in which the veins run- been used previously as cell-specific markers to analyze ning the length of the leaf are surrounded by two layers patterns of leaf development (Mayfield and Taylor 1984; of photosynthetic cells (Brown 1975). The inner bundle Nelson et al. 1984; Aoyagi and Bassham 1986b; Langdale sheath (BS) cells form a single layer around each vein, et al. 1987}. Immunolocalization assays have shown that and the outer mesophyll (M) cells form a layer that is in BS and M cells accumulate C4 enzymes in the same 106 GENES& DEVELOPMENT2:106-115 © 1988 by Cold Spring Harbor Laboratory ISSN 0890-9369/88 $1.00 Downloaded from genesdev.cshlp.org on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Photosynthetic development in maize order as the leaf vasculature differentiates (Langdale et al. 1987). BS and M cells around the median vein mature 1 2 3 4 first (acropetally); cells around the lateral veins then de- velop both acropetally and basipetally. Finally, cells around the intermediate veins mature basipetally. This is the same order in which the cells become morphologi- cally differentiated (Esau 1942; Sharman 1942; Russell and Evert 1985), which is suggestive of a requirement for -95 kd some degree of morphological distinction coincident with or prior to C4 enzyme accumulation. The relative timing of these events cannot be distinguished using C4 proteins as cell-specific markers because we have shown previously that C4 proteins are detected concurrently -~ ~ ..... 75 with the appearance of Kranz anatomy (Langdale et al. 1987). To study earlier developmental events, the corre- sponding C4 mRNAs can be used as markers for each cell type. One report showed that RuBPCase mRNAs ac- cumulate prior to morphological differentiation of BS cells, but PEPCase mRNA accumulates only when Kranz anatomy is fully apparent (Martineau and Taylor -45 1985). These Northern blotting experiments, however, provided only an evaluation of mRNA accumulation within a section of a leaf and not within individual cells of that section. In this paper we examine the cellular expression of C4 Figure 1. Hybrid-selection translation of ME cDNA. Lanes mRNAs during leaf development. We show the spatial exhibit in vitro translation products from reactions with total pattern of C4 mRNA accumulation throughout the leaf leaf poly(A)+ RNA (immunoprecipitated with ME antiserum) and demonstrate that fully differentiated Kranz anatomy (lane 1), RNA hybrid selected with the ME cDNA (lane 2), RNA is not required for the expression of all the C4 mRNAs. hybrid selected with pBS( + ) vector DNA (lane 3), and no RNA Our analysis of the maize mutant argentia (ar)(Eyster added (lane 4). (--*) The 75 kD ME precursor protein. The 95- 1933) shows that BS and M cells always develop in and 45-kD polypeptides are nonspecific products of the transla- tion reaction. clusters across the leaf, which is indicative of interac- tions between the two cell types during development. We also use this mutant to show that BS cells sur- cDNA probes were used as controls to check the purity rounding any individual vein can accumulate C4 of the cell preparations. We detected a single ME tran- mRNAs asynchronously. script, 2.2 kb in size, BS cell specific, and less abundant relative to PEPCase and Ssu transcripts. Results Cellular localization of C4 mRNAs in normal leaves Isolation of a ME cDNA clone Each C4 mRNA exhibited a distinct spatial distribution To study the accumulation of ME mRNA in parallel throughout the leaf. This cellular localization of C4 with other C4 mRNAs, we cloned a partial maize cDNA mRNAs was examined by in situ hybridization of la- as described in Methods. The identity of the cDNA was beled antisense RNA probes to serial sections of normal confirmed by hybrid selection translation reactions with leaf blades (Fig. 3a). The cell-type distribution is consis- the cDNA subclone pBF1 (Fig. 1). The selection-trans- tent with Northern blot data; ME and RuBPCase large lation product (lane 2) was approximately 75 kD, which subunit (Lsu) transcripts were localized in BS cells, and corresponds to the size of the ME precursor protein re- PEPCase mRNA was detected in M cells. Ssu transcripts ported previously (Collins and Hague 1983). were also restricted to BS cells (data not shown). Because all probes were labeled to approximately the same spe- cific activity, the relative abundance of each of these Cell-specific accumulation of C4 mRNAs in normal messages can be estimated by comparing autoradiograph leaves exposure times. Lsu assays were autoradiographed for 12 RuBPCase and PEPCase mRNAs have been detected hr, whereas ME, PEPCase, and Ssu reactions were auto- previously in specific cell types of maize leaves (Link et radiographed for 72 hr. Control reactions using sense la- al. 1978; Martineau and Taylor 1986). To investigate the beled RNA probes exhibited only a low level of nonspe- size, abundance, and cellular location of ME mRNA, we cific hybridization (Fig. 3b). hybridized the ME cDNA probe to poly(A) ÷ RNA iso- Because maize leaves present a developmental gra- lated from whole leaf tissue and from separated cells dient from base (young) to tip (old)(Sharman 1942), we (Fig. 2). PEPCase and RuBPCase small subunit (Ssu) examined the accumulation of specific mRNAs at pro- GENES & DEVELOPMENT 107 Downloaded from genesdev.cshlp.org on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Langdale et al. T BS M tained for Lsu and PEPCase are shown in Figure 5. Spe- cific hybridization of Lsu mRNA was only detected in ~ PEPCase the first leaf, in cells around major veins.
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