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Plant Biology Department, University of Georgia, Athens, Georgia 30602
1 Corresponding author: Plant Biology Department, 4615 Miller Plant Sciences Bldg., University of Georgia, Athens, GA 30602.
E-mail: mjscanlo{at}plantbio.uga.edu
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ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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-helices that are twisted to form a super coil, the coiled-coil motif is a dominant feature in many protein::protein interactions (BURKHARD et al. 2001; YU 2002). EMP2 homologous proteins are found throughout the eukaryotic domain and were first identified in humans as the HEAT SHOCK FACTOR BINDING PROTEIN1 (HSBP1) via binding interactions with HEAT SHOCK FACTOR1 (HSF1) protein (SATYAL et al. 1998; FU et al. 2002; TAI et al. 2002). HSF1 is a transcription factor that induces the expression of a wide range of heat shock protein genes (hsp) during thermal stress (WIEDERRECHT et al. 1988; PIRKKALA et al. 2001). This heat-induced, upregulated transcription of hsp's and other chaperonins is termed the heat shock transcriptional response (HSTR) and is likewise an extraordinarily conserved phenomenon in nature (LINDQUIST 1986; GURLEY and KEY 1991; MORIMOTO 1998). Previous analyses in humans and Caenorhabditis elegans suggest that HSBP1 binds to and inactivates animal HSF1 during attenuation of the heat shock response (SATYAL et al. 1998). These studies suggest that the coiled-coil domain of HSBP1 plays an integral role during mediation of protein::protein interaction with animal HSF1, although no mutant phenotype is observed in null mutations of hsbp1 in C. elegans (SATYAL et al. 1998; TAI et al. 2002). Two HSBP homologs are present in maize: EMP2 and HSBP2. Preliminary investigations of EMP2 suggest a conserved function in HSTR regulation during maize embryogenesis (FU et al. 2002). Loss-of-function emp2 mutants exhibit early staged embryo abortion. The developmental timing of emp2 embryo lethality correlates with the initial competency of maize embryos to invoke the HSTR and with overexpression of hsp transcripts. However, emp2 mutant embryos display aberrant morphology throughout their abbreviated development, well before hsp overexpression and prior to embryonic abortion. Thus, an additional developmental function(s) of EMP2 is implied, outside of its role in HSTR regulation.
In this report, we demonstrate that the accumulation of the maize paralogues EMP2 and HSBP2 is differentially regulated in embryos and leaves. To investigate whether the paralogues function nonredundantly during postembryonic maize development, clonal sectors of emp2 mutant tissue were generated in developing maize shoots against a heterozygous nonmutant background. In contrast to the phenotype seen in emp2 mutant embryos, EMP2 is not required for normal regulation of hsp gene expression in leaves. Furthermore, numerous developmental mutant phenotypes correlate with emp2 mutant sectors in the maize vegetative shoot. Thus, this clonal sector analysis has successfully separated the function of EMP2 in HSTR regulation from its unrelated function(s) during maize shoot development. These data suggest that the EMP2 coiled-coil motif has been recruited to mediate additional protein::protein interaction(s) during the evolution of maize shoot development and that EMP2 and HSBP2 perform nonredundant functions during postembryonic as well as embryonic development.
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MATERIALS AND METHODS |
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Antibody production, recombinant protein expression, immunoblot analysis, and immunolocalization:
Soluble proteins from maize tissues were prepared as described previously (FU et al. 2002). Recombinant proteins of EMP2 and HSBP2 were expressed separately in the pTriplEx vector (CLONTECH, Palo Alto, CA) and in the pBAD TOPO TA vector (Invitrogen, Carlsbad, CA) according to the manufacturers' recommendations. Bacterial protein preparation, protein gel electrophoresis, transfer, and Coomassie blue staining (brilliant blue R350) were performed according to standard methods (SAMBROOK and RUSSEL 2001). Thirty micrograms of total protein was loaded per lane.
Rabbit anti-EMP2 (described in FU et al. 2002) and anti-HSBP2 specific polyclonal antibodies were produced and affinity purified by BioSource (Camarillo, CA). The specificities of the purified antibodies were assayed by ELISA and Western gel blotting against unique multiple antigenic peptides and recombinant proteins of HSBP2. The dilutions used for primary antibodies in Western gel blot assays were 1/3000 (anti-EMP2) and 1/2000 (anti-HSBP2). Fixation, paraffin embedment, sectioning, and immunolocalization of EMP2 antigen in maize kernels were carried out as described by SYLVESTER and RUZIN (1994). The affinity-purified anti-EMP2 polyclonal antibodies were used as the primary antibodies at 1/100 dilution; the secondary antibodies were either goat anti-rabbit IgG-AP conjugated at 1/500 dilution (Promega, Madison, WI) or fluorescein isothiocyanate-conjugated goat anti-rabbit antibody at 1/30 dilution (Jackson ImmunoResearch, West Grove, PA). The images were obtained using a Zeiss Axioplan II equipped with a Southern Micro Instruments (Pompano Beach, FL) CCD camera.
Genetic stocks, sector generation, stress treatment, and analyses:
Maize stocks heterozygous for the emp2-R (reference allele; SCANLON and FREELING 1997; FU et al. 2002; previous designation emp2-1047, SCANLON et al. 1994) in coupling with the albino mutation w3 were obtained by crossing plants of the genotypes W3, Emp2/W3, emp2-R x w3, Emp2/W3, Emp2. One-quarter of the kernels obtained from this cross will be w3, Emp2/ W3, emp2-R. Plants of this genotype were identified by the segregation of both white and emp mutant kernels on self-pollinated ears; these plants were also outcrossed to B73. The progeny were subjected to an additional round of self-pollination and outcrossing to identify individual plants that harbored the emp2 and w3 mutations in coupling. Outcross progeny of the w3, emp2-R heterozygous mutant parents were utilized for clonal analyses. All white sectored plants utilized in this report were analyzed by genomic PCR (FU et al. 2002) to verify that they harbored the emp2-R mutation.
A total of 9000 seeds were imbibed overnight, germinated for 2 days, and subsequently irradiated at 1250–1500 rads utilizing cobalt 60 and average energy 1.25 MeV. Following radiation, 6000 seedlings were field planted, 2000 seedlings were grown at 25° in the greenhouse, and an additional 1000 seedlings were subjected to daily heat stress treatments (36° or 42° for 2 hr).
Single-leaf sectors appeared on juvenile leaves only and were harvested before plant maturity. In contrast, multiple-leaf sectors were harvested at plant maturity. All sectored plants were genotyped by PCR. Hemizygous, w3, emp2/– sectored plants were analyzed to determine the tissue layers occupied by the sectors; phenotypes were scanned, photographed, or photocopied as described (SCANLON 2000).
The position and width of each leaf sector was recorded relative to the lateral vein number at which the sector started and how many lateral veins the sector spanned relative to the number of total lateral veins contained within the half leaf. The lateral vein data were used to extrapolate positions of sectors on mature leaves back to the leaf primordium (Figure 1B), because lateral veins are evenly spaced in young primordia (SHARMAN 1942). When mixed cell layer sectors were encountered, only the sector portion that occupied the full L2-derived layer was mapped in Figure 7. For those cases wherein a narrow leaf phenotype was associated with a sector, the vein number on the nonphenotypic side of the leaf was used as the total vein number. Leaf primordia were assumed to be uniform in size, comprising 40 units in length from midrib to margin (Figure 1B). The overall distribution of sector positions on leaf primordia is presented as overlaying solid lines, with their positions and lengths correlated to the location and width of each sector. Consequently, a two-dimensional plot was derived to describe the correlation of narrow leaf phenotypes with the lateral location of sectors extrapolated to the leaf primordium.
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RESULTS |
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Western gel blot analyses confirmed that no EMP2 protein is detectable in emp2 null albino sectors, although EMP2 does accumulate in sectors hemizygous for the nonmutant Emp2 allele (Figure 4). These data reveal that the emp2-R allele is a null mutation in maize leaves as well as in embryo, although the paralogous protein HSBP2 accumulated to equivalent levels in both emp2 null and nonmutant albino sectors (data not shown). Therefore, the accumulation of EMP2 and HSBP2 is not coregulated in maize leaves.
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Ligule/auricle displacement sectors:
Grass leaves contain a distal blade and a proximal sheath, which are separated by the ligule/auricle structures (SHARMAN 1941). The ligule is an epidermis-derived elaboration of fringe-like tissue on the adaxial leaf surface of the sheath/blade boundary. The auricle is a V-shaped structure that initiates from two points on either side of the midrib and expands outward toward each margin (SYLVESTER et al. 1990). Development of the ligule and auricle is temporally correlated and genetically inseparable (HARPER and FREELING 1996).
There were 11 emp2 null sectors traversing the ligule and auricle that disrupted the continuity of these structures (Figure 6A). Specifically, the ligule/auricle was interrupted at the boundary between the midrib side of nonmutant tissue and the mutant sectored tissue, but it was continuous across the marginal side boundary of the sector. A second ligule/auricle initiated de novo on the midrib side boundary of the mutant sector. The newly initiated ligule/auricle was always displaced proximal to the original auricle and extended laterally to the leaf margin. Although sectors of liguleless1 (lg1) mutation also caused proximal displacement of the ligule/auricle structure, the displacement occurred on the nonmutant tissue lying marginal to the sectored mutant tissue (BECRAFT and FREELING 1991). Within the lg1 mutant sectored tissue the ligule/auricle structure was completely removed (BECRAFT et al. 1990).
As shown in Tables 1 and 2, ligule/auricle displacement phenotypes are associated with both meristematic and nonmeristematic emp2-R/– hemizygous sectors. Although the majority of ligule/auricle sectors (9 of 11) extended through all L2-derived tissue layers (Figure 6B) of the leaf, 2 of the ligule sectors occupied only the adaxial L2-derived leaf tissues (Figure 6C). These data suggest that the correct proximodistal positioning of the adaxial ligule/auricle requires EMP2 function in L2-derived adaxial leaf tissues.
Abnormal phyllotaxy sectors:
Maize leaves initiate in an alternate phyllotaxy; successive leaves arise 
180° apart and offset in two ranks. However, eight cases of abnormal phyllotaxy were observed in emp2 mutant sectored plants, in which successive nodes were not located on opposite sides of the stem. The degree of deviation from the 180° divergence angle varied among different sectored plants. These included cases wherein two successive leaves arose on the same side of the plant; in extreme cases two leaves arose from a single node. In the example shown in Figure 6D (Table 3, sectors 66 and 67) only one of these leaves (L14) contained a midrib, and both leaves are arranged in an abnormal phyllotaxy with respect to the previous leaf. In all cases in which a leaf arose in an abnormal phyllotactic pattern, either the affected leaf or the previous leaf contained two, separate emp2-R/– sectors located on opposite sides of the midvein (Table 3; Figure 6D). These data indicate that the sectors that generated phyllotaxy phenotypes were present at or prior to the founder cell stage of leaf development. Finally, although the majority of these phenotypes arose from sectors marking all L2-derived tissue layers, two partial L2-derived sectors also conferred this phenotype (Table 1). These partial L2-derived sectors reveal that EMP2 function is required in all cells throughout the meristematic L2 tissue layer to establish normal leaf phyllotaxy.
Narrow leaf sector phenotypes:
Plant leaves are composed of at least two mediolateral zones: a central domain, which includes the midrib and leaf tip, and a lateral domain that includes the lower leaf margins. In this clonal analysis, we observed 28 cases of lateral leaf domain deletion phenotypes (Table 1). The emp2-R mutation may correlate with either complete deletion of the lateral leaf domain (i.e., comprising the blade and sheath; 17 cases) or partial deletion of the lateral leaf domain (i.e., comprising the blade alone or blade plus distal sheath; 11 cases).
Representatives of the complete lateral domain deletion phenotypes are depicted in Figure 6, E and F. As shown in Figure 6E, the sheath and proximal blade of the emp2/– null sectored half leaf are much narrower and contain fewer lateral veins than do the unsectored counterparts. Nonmutant leaf blade margins develop distinctive sawtooth hairs and a nonchlorophyllic, tapered edge (Figure 6H), whereas transverse sections of the emp2/– sectored narrow leaf margins revealed blunted, chlorophyllic leaf edges and the absence of sawtooth margin hairs (Figure 6G). Margin structures were normal, however, in sectored regions of the upper leaf blade. These observations are consistent with previous reports (SCANLON et al. 1996) demonstrating that margins of the upper leaf are derived from a different leaf compartment (i.e., the central domain) than are margins of the lower leaf.
The emp2 null albino sectors also gave rise to less severe narrow leaf phenotypes in which the sectored side of the leaf contained fewer lateral veins, yet developed normal margin structures. The sectored sheath either was unaffected or contained a partial deletion that was constrained to the distal sheath region. Furthermore, four sectored narrow leaves were each attached to an accessory leaf (Figure 6J); fusion of the narrow leaf to the accessory leaf occurred in the sheath epidermis (data not shown). The accessory leaves were composed of either sheath plus blade or sheath alone and were positioned immediately adjacent to the corresponding narrow leaf on the node. The accessory leaf phenotype was associated with only meristematic emp2/– null sectors marking the L2-, but not the L1-derived layers (Tables 1 and 4). In addition, two sectored narrow leaves were associated with abnormal outgrowths of sheath tissue that contained highly branched, reticulated, and discontinuous vasculature near the blade sheath boundary of the leaf (Figure 6K). The sheath outgrowth phenotypes correlated with complete L1–L2 layered sectors.
The 28 cases of narrow leaf phenotypes were associated with a total of 23 emp2 null sectors. Only meristematic sectors and nonmeristematic sectors that extended into both sheath and blade conferred narrow leaf phenotypes (Tables 1 and 4). This suggests that EMP2 function is required prior to the completion of early leaf primordial development, after which time these proximal-distal leaf compartments become clonally distinct (POETHIG and SZYMKOWIACK 1995). In addition, all narrow leaf sectors displayed fully albino internal (L2-derived) tissue layers, suggesting that the EMP2 function in a subset of L2-derived tissues is enough for the elaboration of the lateral leaf domain. Finally, although the majority of narrow leaf sectors were astride the abnormal leaf edge (Figure 6E), some sectors were internal to the margin (Figure 6, F and G).
The expression of narrow leaf phenotypes correlates with the lateral position of emp2 null albino sectors:
Although immunohistolocalization analyses of developing maize shoots reveal equivalent accumulation of EMP2 protein throughout all maize tissues examined (Figure 3), a correlation between sector position and the narrow leaf phenotype suggested a compartmentalized function(s) of EMP2. To identify the location of this putative EMP2 functional domain, the lateral positions of narrow leaf phenotypic and nonphenotypic emp2/– null sectors were compared. However, the nonuniform, postprimordial expansion of different regions of the maize leaf precluded direct comparison of sector positions within mature leaves (STEFFENSON 1968; POETHIG 1986). Therefore, the sector locations were compared using lateral veins as a reference for sector positioning (Figure 7; SCANLON and FREELING 1997; see MATERIALS AND METHODS). Lateral veins are established and evenly spaced during early stages of maize leaf development (SHARMAN 1942; BOSABALIDIS et al. 1994) and thus are good indicators of sector position within young leaf primordia. As shown in Figure 7A, the vast majority (24/28) of narrow leaf mutant sectors were contained on the marginal half of the mutant leaf; this region is termed the emp2 phenotypic domain. The clustering of phenotypes within the emp2 phenotypic domain reveals a localized EMP2 function, instead of uneven distribution of emp2 null sectors (Figure 7B).
The fact that not all sectors located within the emp2 phenotypic domain conditioned mutant phenotypes suggests that additional factors, such as the timing of sector induction (Table 1), are important for the expression of narrow leaf phenotypes. For example, whereas all meristematic emp2 null sectors within this domain yielded narrow leaf phenotypes, many postmeristematic sectors did not. In addition, the exact location of EMP2 function is not fixed from meristem to meristem, as discussed below. The mapped location of the emp2 phenotypic domain prompted us to investigate whether EMP2 functions within the lateral meristem domain, a region whose boundaries are marked by foci of NARROW SHEATH (NS) function and expression (SCANLON 2000; NARDMANN et al. 2004). Correspondingly, the emp2 null phenotypic domain was also mapped onto the shoot meristem by determining the meristematic positions of phenotypic and nonphenotypic multiple-leaf sectors (see MATERIALS AND METHODS). As shown in Figure 8, all multiple-leaf sectors associated with narrow leaf phenotypes were localized to the emp2 phenotypic domain, whereas nonphenotypic sectors were all restricted from this region. Interestingly, the emp2 null phenotypic domain overlaps with and extends beyond the NS foci. As the meristem proceeds from middle to adult stages of vegetative development the position of the emp2 null phenotypic domain recedes laterally toward the midrib; a similar phenomenon was observed for the NS foci (SCANLON 2000). It was also noted that the severity of the narrow leaf phenotype correlates with the lateral position of the emp2 null albino sector. That is, emp2 null sectors within the NS foci were mainly associated with a complete lateral domain deletion phenotype (Figures 6, E and F, and 8). In contrast, sectors within the emp2 phenotypic domain, but outside the NS focus, caused only partial domain deletion phenotypes (Figures 6I and 8).
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DISCUSSION |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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Although EMP2 seems to not have an essential role in regulating the HSTR in maize leaves, it does have important, nonredundant functions during maize shoot development. As reported above, a diverse array of developmental defects associate with the sectored loss of EMP2 function in maize shoots, whereas all nonmutant Emp2/– sectors included in our analysis were nonphenotypic. Previous mosaic analyses with the w3 allele also demonstrated that albinism, as well as hemizygosity for most of chromosome arm 2L, does not condition these observed developmental defects in maize shoots (FOSTER et al. 1999; SCANLON 2000). Thus, these phenotypes were specifically linked to the emp2-R mutation.
Heat stress treatment at specific developmental stages is known to induce diverse developmental defects in Drosophila (MITCHELL and LIPPS 1978; PETERSEN and MITCHELL 1987). Likewise, the aberrant expression of hsp90 caused dwarfism, radial symmetrical leaves, and missing leaves in Arabidopsis (QUEITSCH et al. 2002). The requirement of EMP2 during regulation of hsp gene expression in maize embryos initially led to the hypothesis that the range of emp2/– null sector phenotypes observed in this study resulted from aberrant hsp expression: corn plants in the field are often heat stressed and the emp2 null sectors may not be able to attenuate the HSTR. However, EMP2 is not required to regulate the heat shock response in young leaves (Figure 5), nor did we detect aberrant expression of non-heat-inducible hsp's in emp2 null sectors (data not shown). More importantly, we found that the growth temperature and stress treatment of the sectored plants did not affect the range of phenotypes conferred by the emp2 null sectors (data not shown). Therefore, the developmental defects in emp2/– null sectored plants are not caused by a defective heat shock response, suggesting that additional functions of EMP2 are involved in the observed mutant phenotypes. Taken together, genetic and molecular analyses presented herein successfully demonstrated the functional divergence of the maize paralogous proteins EMP2 and HSBP2. EMP2 has evolved additional functions, which are distinct from its conserved function in regulating the HSTR.
Distinct functions of EMP2 during maize shoot development:
Sectored loss of EMP2 function in the postembryonic shoot can lead to the deletion of a leaf domain, displacement of the ligule and auricle, or altered phyllotaxy (Figure 6). One possible explanation of these results is that the tissue loss and tissue/organ displacement phenotypes are caused by a generalized emp2 mutant defect that causes cell death or lack of cell proliferation in sectored tissues. However, several features of the emp2 mutant sectors fail to support this hypothesis. For example, there is no evidence of cell death associated with emp2 null sectored shoot tissue. In contrast, the emp2 null sectored tissues are expansive and morphologically healthy (Figure 6). In addition, the number of cell files between sectored lateral veins is equivalent to that observed in adjoining, nonsectored tissues (Figure 6, B, G, and H, and data not shown). These data are especially informative because lateral veins in maize are established during early primordial stages (SHARMAN 1942), such that a defect in cell proliferation would be manifested as a reduction in intervein spacing. Thus, the sector data strongly suggest that EMP2 is not required for general cell proliferation or viability in the postembryonic maize shoot, although it may be important for proliferation of some specific cell types. It is also possible that the emp2/– null sectors retard the competency of cells to respond to developmental cues at the appropriate time.
The particular phenotype of any emp2/– null sector is correlated with the developmental timing, lateral positioning, and tissue layer specificity of the mutant sector (Table 1). For example, the altered phyllotaxy phenotype was observed only in cases wherein two separate, L2-derived, meristematic emp2 null sectors straddled the midrib-forming region. Current models of phyllotaxy determination inspired by surgical excision of leaf primordia (reviewed in SNOW and SNOW 1933; WARDLAW 1949; STEEVES and SUSSEX 1989), auxin manipulation of the SAM (REINHARDT et al. 1998, 2000, 2003; VERNOUX et al. 2000), and the phyllotaxy mutation terminal ear1 (VEIT et al. 1998) suggest that existing leaf primordia generate an inhibitory signal(s) to prevent premature leaf initiation. The sector data presented herein suggest that EMP2 is somehow required in the shoot meristem to initiate, propagate, or otherwise respond to this leaf inhibitory signal. Furthermore, the presence of EMP2 protein within any portion of L2-derived tissue on just one flank of the meristem is sufficient to maintain this inhibitory signal and normal phyllotaxy. In another example, previous analyses revealed that the leaf lateral domain is patterned in the shoot meristem by a non-cell-autonomous recruitment function initiating at the NS lateral foci (SCANLON 2000). Likewise, sectored loss of EMP2 function within the emp2 phenotypic domain also correlates with the complete or partial deletion of a lateral leaf region. These data suggest that EMP2 function in the meristem and early leaf primordium is also required for the elaboration of the lateral leaf domain.
We suggest that these emp2 null sector phenotypes are due to the loss of expanded (i.e., non-HSTR-related) functions of the EMP2 coiled-coil domain in the maize shoot. The coiled coil is a common protein motif in nature, and specific coiled-coil domain proteins have been shown to interact with multiple, unrelated protein pairing partners that function in disparate molecular pathways (reviewed in BURKHARD et al. 2001; NEWMAN and KEATING 2003). Currently, we are utilizing yeast two-hybrid and proteomic approaches to investigate the distinct protein::protein interactions of EMP2 and HSBP2 in maize embryos and shoots. Preliminary results suggest that these maize HSBP paralogues do indeed interact differently with maize HSF isoforms and other maize proteins (S. FU, unpublished results). Perhaps the identification of EMP2 interacting proteins will help dissect the molecular pathways governing maize developmental processes such as ligule/auricle positioning, lateral leaf development, and phyllotaxy.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSLITERATURE CITED |
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FOOTNOTES |
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LITERATURE CITED |
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