| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
|
First published online August 26, 2005; 10.1104/pp.105.064295 Plant Physiology 139:204-212 (2005) © 2005 American Society of Plant Biologists Aleurone Cell Identity Is Suppressed following Connation in Maize Kernels1Department of Biochemistry, University of California, Riverside, California 92521–0129
Expression of the cytokinin-synthesizing isopentenyl transferase enzyme under the control of the Arabidopsis (Arabidopsis thaliana) SAG12 senescence-inducible promoter reverses the normal abortion of the lower floret from a maize (Zea mays) spikelet. Following pollination, the upper and lower floret pistils fuse, producing a connated kernel with two genetically distinct embryos and the endosperms fused along their abgerminal face. Therefore, ectopic synthesis of cytokinin was used to position two independent endosperms within a connated kernel to determine how the fused endosperm would affect the development of the two aleurone layers along the fusion plane. Examination of the connated kernel revealed that aleurone cells were present for only a short distance along the fusion plane whereas starchy endosperm cells were present along most of the remainder of the fusion plane, suggesting that aleurone development is suppressed when positioned between independent starchy endosperms. Sporadic aleurone cells along the fusion plane were observed and may have arisen from late or imperfect fusion of the endosperms of the connated kernel, supporting the observation that a peripheral position at the surface of the endosperm and not proximity to maternal tissues such as the testa and pericarp are important for aleurone development. Aleurone mosaicism was observed in the crown region of nonconnated SAG12-isopentenyl transferase kernels, suggesting that cytokinin can also affect aleurone development.
The cereal endosperm, which serves as the major source of storage reserves for the embryo, is composed of the starchy endosperm, basal endosperm transfer cells, and the aleurone, as well as starchy endosperm cell subtypes such as the subaleurone and embryo-surrounding region (Becraft, 2001  ; Olsen, 2001, 2004a). The aleurone layer, composed of cuboidal cells that are cytoplasmically dense, serves as the epidermal layer of the endosperm. Aleurone cells synthesize little starch but contain significant quantities of protein as inclusion bodies in small vacuoles as well as oil and phytin. Subaleurone cells are protein rich and contain fewer and smaller starch granules than do cells of the central starchy endosperm. The basal endosperm transfer cells adjacent to the pedicel facilitate nutrient transport from the maternal tissue to the developing endosperm, whereas the embryo-surrounding region lines the endosperm cavity where the embryo develops and may be involved in promoting embryo growth.
Development of the endosperm initiates following double fertilization, in which one pollen sperm nucleus fertilizes the egg cell to form the zygote and the second nucleus fuses with the two polar nuclei in the central cell of the megagametophyte to form the triploid endosperm (Becraft, 2001
CRINKLY4 (CR4), a receptor-like kinase, is important for aleurone cell fate decision (Becraft et al., 1996
During growth of the maize spikelet, the basic repeating unit of the maize inflorescence, development of an upper and lower floret initiates but the lower floret aborts, leaving only one pistillate floret per spikelet to complete its development (Cheng et al., 1982
The Presence of the Aleurone Layer Is Suppressed along the Fusion Plane of a Connated Endosperm
Inhibition of lower floret abortion in T2 SAG12-IPT maize is partially penetrant (Young et al., 2004
The fusion plane between the two endosperms in connated SAG12-IPT kernels was indicated by the junction of the aleurone layers from the respective endosperms, resulting in a double aleurone layer (Fig. 1, D, E, and G) which persisted for only a short distance along the endosperm fusion plane before the development of one aleurone layer ceased. The size of the aleurone cells increased along the fusion plane as a function of their distance from the junction point (Fig. 1, D and E). The typical cuboidal shape was lost as the aleurone cells increased in size, with some adopting a more starchy endosperm-like shape (Fig. 1E). Development of the remaining aleurone layer ceased further into the endosperm and was replaced by cells that exhibited characteristics of the central starchy endosperm on either side of a fusion plane in which no maternal tissue such as the testa or pericarp was evident (Fig. 1, D, E, G, and H). Isolated putative aleurone cells were present along the endosperm fusion plane further into the interior of the connated endosperm (Fig. 1, D and F). Such cells retained aleurone cell characteristics in that they contained the high protein content and lack of starch granules characteristic of this cell type (Fig. 1F). Rare instances of limited invagination of the aleurone layer into the starchy endosperm were also observed (Fig. 1I). These observations indicate a loss of aleurone cell identity as the cells were displaced from the periphery of the connated kernel.
Aleurone cells are characterized by a high level of protein, oil, inorganic calcium, and phytic acid but no starch granules (Olsen, 2001 To the extent that aleurone layers remained along the endosperm fusion plane, the cells in the layers were protein-rich as indicated by staining with Toluidine Blue O (TBO; Fig. 2, A, F, K, P, and U) and lacked starch granules as indicated by staining with Periodic acid-Schiff's (PAS) reagent (Fig. 2, D, I, N, S, and X). A high level of lipids (in the form of oil) characteristic of aleurone cells was observed in these aleurone cells as indicated by staining with Sudan Black (Fig. 2, D, I, N, S, and X). In addition, the presence of phytic acid and inorganic calcium was observed as indicated following staining with Acriflavine (ACF; Fig. 2, B, G, L, Q, and V) or Alizarin Red S (ARS), respectively (Fig. 2, C, H, M, R, and W). These characteristics were observed in isolated aleurone cells as in contiguous cells of the layer, indicating that these cells had maintained aleurone cell identity. Isolated aleurone cells were sometimes organized linearly along the fusion plane (Fig. 2, U–Y) whereas in rare instances, they lacked organization (Fig. 2, P–T). The proximal association of protein-rich subaleurone cells beneath the aleurone layers present along the endosperm fusion plane was not observed as indicated by the lack of staining by TBO (Fig. 2, A, F, and K) or Aniline Blue Black (ABB; Fig. 2, D, I, and N). Further along the fusion plane when both aleurone layers were absent, those cells bordering the fusion plane, i.e. the outermost cell layer of each endosperm, lacked the protein, oil, inorganic calcium, and phytic acid characteristic of aleurone cells. Instead, cells proximal to the aleurone layers along the fusion plane or that bordered the fusion plane in the absence of the aleurone layers had the low protein content and numerous large starch granules characteristic of central starchy endosperm cells (Fig. 1, D–F). Those cells surrounding isolated aleurone cells also lacked those characteristics associated with subaleurone cells but instead were indistinguishable from central starchy endosperm cells (Fig. 2, P–Y).
The aleurone cell wall differs in composition from that of subaleurone and central starchy endosperm cells which is revealed as a bright yellow in light micrographs in ACF-HCl-stained sections (Fig. 2E). In addition to aleurone cell walls, those of the pericarp also stain a bright yellow. Only cell wall staining of aleurone cells present along the endosperm fusion plane was observed with no indication of pericarp tissue (Fig. 2, E, J, O, T, and Y). No staining was observed of the starchy endosperm cells that bordered the fusion plane (Fig. 2E), indicating that the cells in this region of the fusion plane did not exhibit aleurone cell characteristics. These results indicate that aleurone cell identity was maintained for a short distance from the junction of the connated endosperm but was suppressed further into the interior of the fused endosperm to be replaced by central starchy endosperm cells that did not retain any intracellular or extracellular characteristics of aleurone or subaleurone cells. The absence of subaleurone cells proximal to those aleurone cells that were present along the fusion plane suggests disruption of the normal sequence of cell types in the connated kernels.
Suppression of aleurone cell identity along the abgerminal endosperm fusion plane in connated SAG12-IPT kernels may be a result of the loss of positional cues if a peripheral position is necessary to maintain aleurone cell identity. The suppression of aleurone development might also be a consequence of SAG12-IPT expression. If so, aleurone cell identity should be disrupted in the endosperm periphery to the same extent that it is along the abgerminal fusion plane. To examine this possibility, the development of the aleurone layer and subaleurone in the peripheral regions of the endosperm of connated SAG12-IPT kernels was examined.
Normal development of the aleurone layer and subaleurone was observed for most of the endosperm periphery outside the fused abgerminal face. A lack of aleurone cells at the endosperm periphery, however, was observed in the crown region of connated kernels (Fig. 3, A and C) not seen for control kernels (Fig. 3B). The pattern of loss was phenotypically similar to the aleurone mosaicism described for cr4 mutants (Becraft et al., 1996
In addition to the observed aleurone mosaicism, disruption of the normal sequence of cell types in the periphery of connated SAG12-IPT kernels was observed. In regions where aleurone cell identity was suppressed and the peripheral layer had adopted a subaleurone cell identity, starchy endosperm cells indistinguishable from the central starchy endosperm were observed sporadically at the periphery as indicated by the presence of large starch granules and little protein (Fig. 3, E and J) not observed for the controls (Fig. 3, K, L, O, and R). In regions in which aleurone cells were present at the periphery, starchy endosperm cells indistinguishable from the central starchy endosperm were observed immediately beneath the aleurone cells, surrounded by subaleurone cells (Fig. 3, E, M, and P). To determine whether the observed abnormalities in maintaining aleurone cell identity and starchy endosperm cell specification was specific to the fusion event that resulted in connated kernels, the aleurone layer and subaleurone region in the endosperm periphery of nonconnated SAG12-IPT kernels were examined. These kernels develop from the upper floret whereas kernel development from the lower floret aborts prior to pistil fusion leaving an empty caryopsis which remains unfused with the upper kernel (Fig. 1C). Consequently, the upper floret kernel contains a single embryo and a nonfused endosperm as in wild-type kernels. Aleurone mosaicism was observed in nonconnated SAG12-IPT kernels but was limited to the crown region (Fig. 4). No suppression of aleurone cell identity was observed along the abgerminal side of the kernel, which is the region involved in fusion in connated kernels, or in basal endosperm transfer cells present over the pedicel, or in the embryo-surrounding region (data not shown). The suppression of aleurone cell identity at the periphery sometimes involved a large number of cells (Fig. 4, A–C, E, F, and H) or a few (Fig. 4, D and G).
Disruption of the normal sequence of cell types was observed in nonconnated SAG12-IPT kernels as it was in connated kernels. Suppression of aleurone cell identity resulted in the presence of subaleurone cells (Fig. 4, C, F, and L) or starchy endosperm cells (Fig. 4, I and K) at the periphery. Starchy endosperm cells indistinguishable from the central starchy endosperm were also observed immediately beneath the aleurone layer, surrounded by subaleurone cells (Fig. 4, J, N, and O). Additional aleurone cells were observed occasionally beneath the aleurone layer in the region of the subaleurone (Fig. 4, M and P). These cells exhibited morphological and biochemical characteristics typical of aleurone cells including high protein and lipid content, aleurone cell walls, and lack of starch granules (Fig. 4, M and P). Whether these represent periclinal division of cells in the aleurone layer or differentiation of subaleurone cells into aleurone cells is unknown. These observations suggest a loss of control in the normal sequence of cell types in the outermost region of the endosperm, including the presence of aleurone and central starchy endosperm cells in the subaleurone region.
Alternative models for aleurone specification require signaling from maternal tissues such as the testa/pericarp or degenerating nucellus or from the zygote itself (Olsen et al., 1999 ; Becraft and Asuncion-Crabb, 2000; Becraft et al., 2001; Gifford et al., 2003). In the first model, aleurone cell identity is established by virtue of its position as the cell layer closest to the testa/pericarp where the concentration of the morphogen would be highest. In the second model, aleurone cell identity is established by virtue of its position as the most peripheral cell layer of the endosperm without requiring proximity to maternal tissues, described recently as the surface rule (Olsen, 2004b). The fusion plane of a SAG12-IPT connated kernel in which aleurone layers were positioned between two independent endosperms represents the repositioning of the abgerminal aleurone cell layer from its normal pericarp-proximal position to a position next to the adjoining aleurone cell layer in the connated endosperm. Thus connation results in the internalization of the abgerminal aleurone layer into the center of a single, connated endosperm while maintaining its clonal relationship with the endosperm from which it developed. Aleurone specification along the fusion plane of a connated kernel was suppressed in steps in which two aleurone layers were observed at the endosperm juncture and for 10 to 20 cells into the connated endosperm. This maintenance of aleurone cell identity is in contrast to the respecification of aleurone daughter cells into starchy endosperm cells when displaced internally by just one cell layer following periclinal division (Becraft and Asuncion-Crabb, 2000) but is similar to the maintenance of aleurone cell layers in regions of endosperm invagination of mutants affected in endosperm development (Olsen, 2004b). Following suppression of one aleurone layer within 10 to 20 cells into the connated endosperm, suppression of the remaining aleurone layer occurred within an additional five to 10 cells along the fusion plane, at which point the presence of aleurone cells became sporadic resulting in a few isolated aleurone cells before becoming largely absent. Instances of isolated aleurone cells were observed further into the interior of the connated endosperm but always at the fusion plane, which may represent regions of late or incomplete fusion of the connated endosperm. These observations support the conclusion that peripheral position and not proximity to maternal tissues such as the testa and pericarp are important for aleurone development.
Disruption of the normal sequence of endosperm cell types was also observed. Subaleurone cells were present beneath the aleurone layer of connated kernels up to the point of connation. However, they were absent from their position beneath each aleurone layer along the fusion plane for as far as the aleurone layers persisted, and, instead, starchy endosperm cells were present. Following suppression of both aleurone cell layers along the fusion plane further into the interior of the connated endosperm, only central starchy endosperm cells were present at the fusion plane. These observations support the notion that positional cues are essential for aleurone development. The observation that aleurone cells are largely absent within 20 to 30 cells of separation from the surface of the connated endosperm is consistent with a signal originating at or beyond the endosperm periphery, e.g. from maternal tissues. The development of aleurone cells within 20 to 30 cells of separation from the testa/pericarp suggests that direct contact with maternal tissue is not required, as observed with mutants affected in endosperm development (Olsen, 2004b
The presence of isolated aleurone cells within the interior of the connated endosperm but at the outermost layer of cells of the endosperm from which it developed suggests that even in the absence of any maternally derived signal, position-derived information with respect to the starchy endosperm may be sufficient as aleurone cells that are completely surrounded by starchy endosperm have not been observed in wild-type endosperm. Interestingly, the mutant globby1-1 permits the development of aleurone cells within the starchy endosperm (Costa et al., 2003 The most notable observation resulting from connation was the suppression of aleurone cells along most of the fusion plane, suggesting that the presence of starchy endosperm on either side of an aleurone cell serves to suppress its development either by inhibiting aleurone cell differentiation or by causing aleurone cells to undergo respecification into starchy endosperm cells. Thus, signals originating from the starchy endosperm are likely to be involved in determining the development of aleurone cells at the periphery. It should be noted that such a starchy endosperm-derived signal is not incompatible with the involvement of a maternally derived signal (e.g. produced by the testa/pericarp) that may also contribute to aleurone development.
Cytokinin as a possible candidate for a zygotically derived signal is supported by several observations. Expression of CycD3, which promotes progression through the G1-S transition of the cell cycle, is induced by cytokinin, and overexpression of CycD3 in Arabidopsis eliminated the requirement for exogenous cytokinin during callus growth (Riou-Khamlichi et al., 1999
The observed defects in aleurone development of SAG12-IPT kernels also support a regulatory role for cytokinin during endosperm development. Sporadic suppression of aleurone cell development in the crown region of SAG12-IPT connated and nonconnated kernels resulted in aleurone mosaicism, consistent with other mutants affecting aleurone development (e.g. bareback*, naked*, collapsed2-o12, mosaic1, and paleface*). Whether any of these genes are regulated by cytokinin will be of interest to determine. Cytokinin may have been generated in SAG12-IPT kernels in degenerating maternal tissues or from the endosperm itself as it undergoes cell death (Young and Gallie, 2000 In conclusion, one consequence of the formation of a two-seeded fruit resulting from the connation of adjacent kernels is the suppression of aleurone cell identity along the fusion plane, despite the fact that the relationship between the outermost layer of cells of each endosperm along the fusion plane is maintained with respect to the endosperm beneath it. Thus, the observations made with connated kernels supports the surface rule that aleurone cell identity is established when the most peripheral cell layer is bounded on just one side by endosperm.
Generation of Transgenic Lines
Embryogenic callus from HiII (derived from A188 x B73) was used for transformation by particle bombardment (Gordon-Kamm et al., 1990
Tissue was fixed in formaldehyde-acetic acid (50% ethanol, 5% acetic acid, 3.7% formaldehyde) at 4°C, dehydrated through a graded ethanol series to 100%, and embedded in resin. Plastic kernel sections (3 µm) were stained with TBO or ABB for protein (Lillie, 1977 For SBB staining, section-containing slides were first soaked in freshly made 0.1% bromine in water (v/v) for overnight. The slides were rinsed in water the following day, stained with 3 mg/mL SBB in 70% ethanol for 30 min, and washed with 70% ethanol. Excess ethanol was removed and the slides air-dried overnight. For ABB, sections were stained with 1% ABB, pH 7.0, in phosphate-buffered saline for 30 min and rinsed well in water. Excess water was removed and the slides air-dried overnight. For PAS staining, sections were oxidized in 1% periodic acid for 5 min and continuously washed in water for 3 min. The slides were then placed in a Coplin jar with Schiff's reagent (Sigma) for 10 to 40 s until the appearance of magenta color and were then continuously washed in water for 10 min. Excess water was removed and the slides air-dried overnight. For staining with ACF, sections were stained with 0.5% ACF in water for 1 h, washed in water, blotted, and air-dried overnight. For staining with ARS, sections were stained with 2% ARS in water for 1 h, washed in water, blotted, and air-dried overnight. For staining with LG, sections were stained with 1% LG in water for 10 s, washed in water, blotted, and air-dried overnight. For staining with TBO, sections were stained with 1% TBO in phosphate-buffered saline, pH 7.0, for 10 s, washed in water, blotted, and air-dried overnight. For SBB/ABB/PAS triple staining, sections were stained first with SBB as described above and following washing with 70% ethanol, the sections were rehydrated in water and stained in 1% ABB as described above and finally stained with PAS as described above. For ABB/PAS double staining, sections were stained first with ABB and counterstained with PAS. For ARS/LG double staining, sections were stained first with ARS and counterstained with LG. Images of the stained kernel sections were collected using a light microscope.
The authors thank Dr. Rick Amasino for the pSAG12-IPT construct and Drs. Patricia Springer and Elizabeth Lord for the use of microtomes and microscopes. Received April 15, 2005; returned for revision June 17, 2005; accepted July 7, 2005.
1 This work was supported by the U.S. Department of Agriculture (grant nos. NRICGP 97–35304–4657 and 03–35100–13375), the National Science Foundation (grant no. MCB–9816657), and the University of California Agricultural Experiment Station. 
2 Present address: Department of Biology, University of Western Ontario, London, Ontario, N6A 5B7 Canada. Article, publication date, and citation information can be found at www.plantphysiol.org/cgi/doi/10.1104/pp.105.064295. * Corresponding author; e-mail drgallie{at}citrus.ucr.edu; fax 951–827–4434.
Bayliss OB, Adams CWM (1972) Bromine-sudan black: a general stain for lipids including free cholesterol. Histochem J 4: 505–514[Medline] Becraft PW (2001) Cell fate specification in the cereal endosperm. Semin Cell Dev Biol 12: 387–394[CrossRef][Medline] Becraft PW, Asuncion-Crabb Y (2000) Positional cues specify and maintain aleurone cell fate in maize endosperm development. Development 127: 4039–4048[Abstract]
Becraft PW, Kang SH, Suh SG (2001) The maize CRINKLY4 receptor kinase controls a cell-autonomous differentiation response. Plant Physiol 127: 486–496 Becraft PW, Li K, Dey N, Asuncion-Crabb Y (2002) The maize dek1 gene functions in embryonic pattern formation and cell fate specification. Development 129: 5217–5225 Becraft PW, Stinard PS, McCarty DR (1996) CRINKLY4: a TNFR-like receptor kinase involved in maize epidermal differentiation. Science 273: 1406–1409[Abstract] Brown RC, Lemmon BE, Olsen O-A (1996) Polarization predicts the pattern of cellularization in cereal endosperm. Protoplasma 192: 168–177[CrossRef] Calderon-Urrea A, Dellaporta SL (1999) Cell death and cell protection genes determine the fate of pistils in maize. Development 126: 435–441[Abstract] Cheng PC, Greyson RI, Walden DB (1982) Organ initiation and the development of unisexual flowers in the tassel and ear of Zea mays. Am J Bot 70: 450–462 Christensen AH, Quail PH (1996) Ubiquitin promoter-based vectors for high-level expression of selectable and/or screenable marker genes in monocotyledonous plants. Transgenic Res 5: 213–218[CrossRef][ISI][Medline] Colombo L, Franken J, Van der Krol AR, Wittich PE, Dons HJ, Angenent GC (1997) Downregulation of ovule-specific MADS box genes from petunia results in maternally controlled defects in seed development. Plant Cell 9: 703–715[Abstract]
Costa LM, Gutierrez-Marcos JF, Brutnell TP, Greenland AJ, Dickinson HG (2003) The globby1–1 (glo1–1) mutation disrupts nuclear and cell division in the developing maize seed causing alterations in endosperm cell fate and tissue differentiation. Development 130: 5009–5017 De Block M, Botterman J, Vandewiele M, Dockx J, Thoen C, Gossele V, Movva NR, Thompson C, Van Montagu M, Leemans J (1987) Engineering herbicide resistance in plants by expression of a detoxifying enzyme. EMBO J 6: 2513–2518[ISI][Medline] Fulcher RG (1982) Fluorescence microscopy of cereals. Food Microstruct 1: 167–175
Gan S, Amasino RM (1995) Inhibition of leaf senescence by autoregulated production of cytokinin. Science 270: 1986–1988
Gifford ML, Dean S, Ingram GC (2003) The Arabidopsis ACR4 gene plays a role in cell layer organisation during ovule integument and sepal margin development. Development 130: 4249–4258
Gordon-Kamm WJ, Spencer TM, Mangano ML, Adams TR, Daines RJ, Start WG, O'Brien JV, Chambers SA, Adams WR, Willetts NG, et al (1990) Transformation of maize cells and regeneration of fertile transgenic plants. Plant Cell 2: 603–618 Hotchkiss RD (1948) A microchemical reaction resulting in the staining of polysaccharide structures in fixed tissue preparations. Arch Biochem Biophys 16: 131–141 Lid SE, Al RH, Krekling T, Meeley RB, Ranch J, Opsahl-Ferstad HG, Olsen OA (2004) The maize disorganized aleurone layer 1 and 2 (dil1, dil2) mutants lack control of the mitotic division plane in the aleurone layer of developing endosperm. Planta 218: 370–378[CrossRef][ISI][Medline]
Lid SE, Gruis D, Jung R, Lorentzen JA, Ananiev E, Chamberlin M, Niu X, Meeley R, Nichols S, Olsen OA (2002) The defective kernel 1 (dek1) gene required for aleurone cell development in the endosperm of maize grains encodes a membrane protein of the calpain gene superfamily. Proc Natl Acad Sci USA 99: 5460–5465 Lillie RD (1977) H.J. Conn's Biological Stains: A Handbook on the Nature and Uses of the Dyes Employed in the Biological Laboratory, Ed 9. Williams & Wilkins, Baltimore McGee-Russell SM (1958) Histochemical methods for calcium. J Histochem Cytochem 6: 22–42[Abstract] Morris RO (1997) Hormonal regulation of seed development. In BA Larkins, IK Vasil, eds, Cellular and Molecular Biology of Plant Seed Development. Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 117–149 Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52: 233–267[CrossRef][ISI][Medline] Olsen OA (2004a) Dynamics of maize aleurone cell formation: the "surface" rule. Maydica 49: 37–40[ISI] Olsen OA (2004b) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell (Suppl) 16: S214–S227 Olsen OA, Linnestad C, Nichols SE (1999) Developmental biology of the cereal endosperm. Trends Plant Sci 4: 253–257[CrossRef][ISI][Medline]
Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JA (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Science 283: 1541–1544
Shen B, Li C, Min Z, Meeley RB, Tarczynski MC, Olsen OA (2003) sal1 determines the number of aleurone cell layers in maize endosperm and encodes a class E vacuolar sorting protein. Proc Natl Acad Sci USA 100: 6552–6557
Wang C, Barry JK, Min Z, Tordsen G, Rao AG, Olsen OA (2003) The calpain domain of the maize DEK1 protein contains the conserved catalytic triad and functions as a cysteine proteinase. J Biol Chem 278: 34467–34474 Young TE, Gallie DR (2000) Programmed cell death during endosperm development. Plant Mol Biol 44: 283–301[CrossRef][ISI][Medline] Young TE, Giesler-Lee J, Gallie DR (2004) Senescence induced expression of cytokinin reverses pistil abortion during maize flower development. Plant J 38: 910–922[Medline] This article has been cited by other articles:
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
| ASPB Publications | PLANT PHYSIOLOGY | THE PLANT CELL | |
|---|---|---|---|
TOP
ABSTRACT
RESULTS
