Department of Plant and Microbial Biology, University of California, Berkeley, CA 94720, USA
*Author for correspondence (e-mail: freeling{at}nature.berkeley.edu)
Accepted 25 June 2002
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SUMMARY |
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Key words: Maize, Leaf development, Rolled leaf1 (Rld1), Dorsoventrality
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INTRODUCTION |
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The maize leaf and all other lateral organs develop from populations of segment founder cells in the shoot apical meristem (Scanlon et al., 1996). Along the proximodistal (tip to base) leaf axis there are three readily visible regions of the maize leaf: proximal sheath, ligule/auricle region and distal blade (Fig. 1A). The dorsoventral axis contains five tissue layers (TL) that run continuously through the three regions of the proximodistal axis. The DV axis cuts through three tissue layer types: the outer epidermal layers (TL1 and TL5), the middle mesophyll and vascular layer (TL3), and the ground mesophyll layers (TL2 and TL4), as diagrammed in Fig. 6. The adaxial epidermis (TL1) and the abaxial epidermis (TL5) of the leaf have distinct epidermal cell type patterns (Freeling and Lane, 1993
). The leafs adaxial epidermis (TL1) can be distinguished by longitudinal files of macrohairs, which are large single cell hairs that occur in files of bulliform cells running parallel to the proximodistal axis of the blade. The adaxial surface of the leaf is also marked by the presence of ligule tissue at the blade sheath boundary. The abaxial epidermis (TL5) contains none of these features. The middle tissue of the leaf also shows dorsoventrality. Veins contain polarized xylem and phloem. Wild-type leaves also have a characteristic DV pattern of hypodermal schlerenchyma, which are specialized structural ground tissue cells associated with veins.
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In this paper we introduce and characterize the semi-dominant mutants of the maize rolled leaf1 (rld1) gene. The allele we use most often is Rld1-O. The phenotypes of the group of mutant alleles are very similar in almost all aspects of the phenotype and we refer to this group of mutants as Rld1 mutants. The characteristic tissue pattern associated with the maize leaf is abnormal and can broadly be defined as being misspecified along the dorsoventral axis. We will show that Rld1 alleles act in one epidermis, but can switch the DV polarity of the entire leaf.
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MATERIALS AND METHODS |
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Microscopy
Autofluorescence
To examine internal leaf architecture, transverse hand-cut sections were observed on a Zeiss standard light microscope under epifluorescent illumination using a 395-440 nm excitation filter with a 470 nm long pass observation filter.
Staining of vascular bundles
Tissue from [P8]/[P9] (the 8th or 9th leaf away from the meristem) adult leaves were vacuum infiltrated for 20 minutes in a 3:1 ethanol/acetic acid fixitive and left at room temperature overnight. The tissue was then transferred into a 0.5% sodium metabisulfite solution for several hours. Subsequently the tissue was transferred into a diluted Schiffs reagent (0.1 % basic fuschin, 1.9% in 15:85 1N HCl/water) and shaken for several hours. 200 mg activated charcoal is then added to destain tissue. After Schiff staining, the tissue is returned to a sodium metabisulfite solution (0.5%) overnight. The tissue is dehydrated through an ethanol series followed by several changes of absolute ethanol. The samples are then placed in a Petri dish filled with ethanol and viewed using a dissecting microscope using methods adapted from Cheng (Cheng, 1995).
Epidermal impressions
Impressions were made to examine the epidermis of wild-type and Rolled leaf1 mutant leaves. As suggested by L. Smith, UCSD, San Diego, USA, a drop of cyanoacrylate glue, (Quick Tite super glue) was placed on a glass slide and leaf tissue was pressed into it. Once the glue had dried, tissue samples were removed and slides were examined using (DIC) optics on a Zeiss standard light microscope.
Dosage analysis
The B-A translocation stocks, TB-9Lc and TB-9La, were obtained from the Maize Genetics Cooperative. Rolled leaf1-O and Rolled leaf1-1608 heterozygotes were crossed as females by each B-A translocation stock. Our results from these two alleles were consistent, and pooled. Maize B chromosomes are supernumerary chromosomes that exhibit meiotic drive; the A chromosomes are the normal genetic complement of the maize genome. The B chromosome centromere often undergoes mitotic nondisjunction in the second microspore division resulting in sperm that are hyperploid and hypoploid for the A arm of the B-A translocation. This allows us to generate an aneuploid series, as the progeny of this cross segregate for genotypes Rld1-O/, Rld1-O/+, Rld1-O/++, rld1+/, rld1+/+, rld1+/++ where + is a 9L arm carrying a wild-type rld1 allele and is no arm 9L at all.
Mosaic sector analysis
A stock carrying the albino mutant white luteus4-R (wlu4-R), which maps approximately 45 map units proximal to rld1 on chromosome 9L, was obtained from the Maize Genetics Coop. Plants heterozygous for wlu4 were crossed onto heterozygous Rolled leaf1-O mutants. These crosses generated families segregating 1:1:1:1 for Rld1-O Wlu4+/rld1+ wlu4, rld1+ Wlu4+/rld1+ wlu4, Rld1-O Wlu4+/rld1+ Wlu4+ and rld1+ Wlu4+/rld1+ Wlu4+. Seven thousand five hundred seeds from these crosses were allowed to imbibe on paper towels for 24 hours at 30°C. From 50-100 seeds were transferred onto two moist Whatman filter papers in a 100 mm Petri dish. Imbibed seeds were irradiated with 1500 rads for approximately 7 minutes through a 0.21 mm Cu and 1.0 mm Al filters with a 160 kV Pantak X-ray machine run at 250 kV at Lawrence Berkeley Labs, Berkeley, CA. The irradiated seeds were planted in the summer nursery at the Gill Tract Field of UC Berkeley in Albany, CA.
Throughout development, plants were screened for albino sectors and sectored leaves were collected at maturity. These clonal sectors were presumed to be aneuploid for the albino marker (wlu4/). Examination of nonmutant sibs (rld1+ Wlu4+/rld1+ wlu4) showed that the partial loss of chromosome 9L did not affect the morphology of the mature leaf. A total of 32 Rld1-O plants were found to contain sectors and were examined for the Rolled leaf1 phenotype in and around the sector. Leaf number, sector width and position, color and shape were recorded for each sector and sectors were drawn schematically. Transverse sections of these leaves were made by hand. Observations were made on a Zeiss standard light microscope under epifluorescent illumination, using a 395-440 nm excitation filter with a 470 nm long pass observation filter as described previously (Becraft and Freeling, 1994). Using these conditions, normal green chloroplasts fluoresce red and chloroplasts in albino tissue fluoresce a light yellow. All mesophyll layer cells contain chloroplasts. The genotype of the epidermal layers were determined by examining the chlorplast-containing guard cells. Since chromosome loss can occur in varying tissue layers, we recorded the phenotype within and near white sectors and which tissue layers (TL1-TL5) were affected. Blade sectors were scored for the presence and position of epidermal macrohairs and hypodermal schlerenchyma. Juvenile leaves were not analyzed because they lack epidermal macrohairs. White sectors and surrounding tissue layers were scored using these phenotypes as being either Rolled leaf1 or non mutant.
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RESULTS |
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Abaxial ligule flap and irregular venation patterning
The blade-sheath boundary of wild-type leaves is marked by the presence of a ligule. The ligule is continuous along the adaxial surface from margin to margin. All Rolled leaf1 mutant alleles result in leaves with an abaxial ligule flap in addition to the adaxial ligule (Fig. 1C). That is, the ligule domain at the blade/sheath boundary in Rld1 mutants is adaxialized on both epidermal surfaces and never displays the switching seen with the macrohairs. The expressivity of this abaxial ligule flap phene changes from plant to plant and leaf to leaf of the same plant. The abaxial ligule flap varies in width, sometimes extending from margin to margin and other times being just a few millimeters in width. When the abaxial ligule flap does not extend across the entire width of the blade, the flap becomes a pair of flaps placed symmetrically on either side of the midrib.
Proximal and distal to the pair of ectopic ligule flaps, Rolled leaf1 mutant leaves display varying degrees of pale tissue extending from the ligule flap into both the blade and sheath (Fig. 3A). The ground tissue cells in these pale sectors were not green, suggesting absence of chloroplasts or chlorophyll. We compared wild-type vasculature with mutant Rolled leaf1 leaf vasculature. Wild-type leaf blade and sheath display a regular parallel pattern of lateral veins separated by many intermediate veins in the blade and at least one intermediate vein in the sheath (Fig. 3B,D). In addition, there are transverse vascular bundles running horizontally between the lateral and intermediate veins (Fig. 3B,D). The pale tissue or clearing found in mutant Rolled leaf1 leaves is associated with lack of development of intermediate and transverse vascular bundles in that region (Fig. 3C,E).
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All aspects of the Rolled leaf1 phenotype are non cell-autonomous in the dorsoventral dimension. We could not definitively measure cell autonomy of the Rolled leaf1 phenotype in the lateral dimension because the markers used are macrohairs and hypodermal schlerenchyma. These markers occur periodically across the lateral dimension and sector boundaries did not always coincide with these markers. Therefore, we cannot eliminate the possibility of lateral signaling that extends for a few cells. However we never saw the Rolled leaf1 phenotype above wild-type abaxial epidermis.
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DISCUSSION |
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Rld1 acts after initial dorsoventrality is established
Rld1 leaves display a partial DV switching of epidermal tissue and ground tissue with a bias towards adaxialization. Polarity appears normal over regions of varying width across the leaf. The affected area may be localized between only two lateral veins or may include several lateral veins. In regions with altered polarity, the tendency is toward adaxial/abaxial (ad/ad) polarity. However, many Rld1 mutants have regions where the epidermal and sub-epidermal tissues have been flipped, giving abaxial/adaxial (ab/ad) polarity to the tissues (Fig. 8). Hay et al. (Hay et al., 2000) found that abaxial fiber cell density was greater in wild-type than in Rld1 mutant leaves, supporting the hypothesis that differential fiber development between the two surfaces produces curvature. Our observations also support the theory that differential schlerenchyma distribution leads to the inward rolling of the leaf. The fact that mutant leaves exhibit dorsoventrality and have normal vascular polarity at inception indicates that rld1+ is not involved in setting up initial dorsoventral polarity but rather in the reception, propagation, or maintenance of this state (Fig. 8).
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Dosage and mosaic analyses suggest rld1+ functions in the abaxial epidermis
To gain insight into how the dominant Rld1 mutant allele functions in relation to the wild-type allele, we performed a dosage analysis. Dosage analysis determines the effect of changing copies of rld1+, in a mutant Rld1 plant. The results of our dosage analysis indicate that addition of rld1+ alleles to a Rld1-O mutant allele reduces the severity of the phenotype. This result suggests that Rld1-O is an antimorph, or dominant negative mutation. Antimorphic dominants are interpreted as mutants that encode a product that antagonizes normal gene activity (Muller, 1932; Poethig, 1988
). Since an antimorph acts by inhibiting the wild-type alleles function, it follows that tissues affected by the mutant phenotype are within the domain of RLD1 function.
The mosaic analysis was conducted on Rld1-O mutants to determine if the phenotype is cell-autonomous or non cell-autonomous and to identify the focus of action of the dominant mutant gene product. Our results indicate that a signal emanating from the mutant abaxial epidermis is able to affect all five tissue layers. This includes altering the characteristic cell types of both epidermal layers (TL1 and TL5), changing the polarity of the hypodermal schlerenchyma in the subepidermal mesophyll layers (TL2 and TL4), and disturbing the formation of intermediate and transverse veins in the middle mesophyll layer (TL3), but this was not closely scored in the mosaic analysis. It is interesting that such a pleiotropic mutant phenotype is caused by a disturbance in a gene that acts within a single cell layer.
rld1+ acts in the abaxial epidermis and is involved in trans-epidermal signaling that reinforces polarity
The data from the mosaic analysis taken with our results from the dosage analysis imply that rld1+ acts in the abaxial epidermis. Our dosage analysis showed that, in Rolled leaf1 mutants, the mutant Rld1 product is competing with the wild-type RLD1. The antimorphic data from the dosage analysis allows us to interpret Rld1 like a loss-of-function mutant. Our mosaic analysis showed the focus of the mutant Rld1 to be the abaxial epidermis. It follows that rld1+ is involved in initiation or maintenance of the abaxial epidermal identity and in propagation or maintenance of the correct polarity of the leafs DV axis. Furthermore, we never find abaxial/ abaxial polarity in Rld1 mutants, supporting our conclusion that rld1+ promotes abaxial identity in the lower epidermis.
The Rld1 mutants also give us a unique insight into the complexity of signaling involved in setting up the correct DV polarity. Our results suggest a transverse signaling mechanism from abaxial epidermis to adaxial epidermis, affecting the polarity of schlerenchyma and veins. The abaxial surface of Rld1 mutant leaves is partially adaxialized and often this is accompanied by the adaxial epidermal tissue directly above being abaxialized. This reversal of epidermal tissue suggests there is communication between the two surfaces, perhaps a polarity maintenance signal (PMS) from one epidermis to the other, reinforcing the other epidermis to be the opposite identity to maintain correct dorsoventral polarity (Fig. 8). It is still undetermined if this signal emanates from the adaxial surface to reinforce abaxial identity or if it emanates from the abaxial surface and reinforces adaxial identity. Yet, switching has never been seen in the ligular region and sometimes does not occur in the blade, thus leading to two adaxial surfaces which are most commonly observed at the boundaries of a switched, ab/ ad, region. However, sometimes homogenous regions of ad/ab polarity exist. Hence our mutant phenotype suggests a two step process for polarity maintenance. In Rld1 mutants first there is mis-specification of the abaxial epidermis to adaxial, and secondly, in some cases, there is reversal of the adaxial epidermis to abaxial identity. Since we do not always see step two (epidermal switching), we hypothesize that timing does not always permit this to occur. The cells of the adaxial epidermis might become determined to that fate and are no longer responsive to the signal from the lower epidermis that has taken on adaxial tissue identity (Fig. 8) or there is a leaky signal still coming from the abaxial epidermis maintaining adaxial tissue identity in the upper tissue layers (not shown). Therefore other factors must influence some part of the Rld1 trans-tissue signaling pathway.
One model for initiation and maintenance of dorsoventral polarity involves three separate steps. Based on the results of surgical experiments suggesting that a factor, a peripheral signal, emanating from the center of the shoot apex is necessary for development of the adaxial domain (Hanawa, 1961; Snow and Snow, 1959
; Sussex, 1954
; Sussex, 1955
), the first step in polarity establishment is dependent on a morphogen, the peripheral/adaxialization signal (PAS), coming from the meristem (the red arrow in Fig. 8). Adaxial factors (AdFs) in the surface of the leaf primordia closest to the meristem are responsible for perception and propagation of this signal to form a flattened leaf and adaxial tissue identity. It is unknown whether the default state is a radial leaf with abaxial identity or if both abaxial and adaxial identities are independently specified through AdFs and abaxial factors (AbFs). If abaxial identity is not the default state of the leaf, it might be established as a response to lower morphogen concentrations or via a signal cascade initiated by the PAS, both of which might involve AbFs. As the developing leaf grows away from the meristem, the source of the PAS, a new mechanism is needed for maintenance of dorsoventral polarity.
Regardless of whether abaxial and adaxial tissues are independently specified, our data proves that they interact in the maintenance of their identities. This second step involves feedback from either of the leaf surfaces to the other in the form of a polarity maintenance signal (PMS): Im adaxial, you be abaxial trans-tissue PMS (Fig. 8) (or I am abaxial, you be adaxial trans-tissue PMS, not shown). RLD1 is involved in the maintenance of the DV axis. RLD1 might be responding to the PMS which signals the abaxial half of the blade primordium to maintain abaxial identity. Alternatively, RLD1 might interact directly or indirectly (via AdFs) with the PAS and inhibit its action in the abaxial epidermis, preventing adaxialization of the lower surface of the leaf . In Rld1 mutants this step results in two adaxial surfaces. Additional genetic support for step two and our interpretation that RLD1 normally abaxializes the most peripheral epidermis comes from double mutants between Rld1 and leafbladeless1 (lbl1). leafbladeless1 mutant plants are abaxialized. Juarez and Timmermans (Juarez and Timmermans, 2001) reported that the double mutant resulted in mutual suppression of both phenotypes as expected if Rld1 adaxialized and lbl1 homozygote abaxialized. However, our data did not show mutual suppression, but did show that Rld1-1441 almost completely suppressed the lbl1-R phenotype whilst the Rld1-1441 phenotype remained strong (J. M. N. and M. F., unpublished).
Our results suggest that sometimes the developmental window still allows the adaxial half of the blade primordia to become abaxialized, suggesting a third step. This third step involves further reinforcement of dorsoventral identity in the developing blade which is no longer receiving any PAS morphogen from the meristem (Fig. 8, late blade primordium). In Rld1 mutants, this switch might either be due to tissue expressing AdFs signaling the opposite side to express abaxial characters, which in the mutant case can not affect the abaxial surface but can affect the adaxial surface (Fig. 8). Or the switch might result from reversion of the adaxial tissue to a default abaxial identity, if the PMS emanating from the abaxial epidermis relies on AbFs which are not expressed in the Rld1 mutant (not shown).
Regarding the developmental time at which of RLD1 acts, we believe our model is supported by the fact that the polarity of the vasculature of Rld1 leaves is normal. This suggests that early in leaf development, during the acropetal and the basipetal waves of vein differentiation, the polarity of the leaf is normal in Rld1 mutants. Based on phenotype and antimorphic data, we propose RLD normally acts following this stage during the differentiation of epidermal-specific and subepidermal-specific cell types which follows vein differentiation.
The occurrence of homogenous ad/ad leaf regions is central to our three-step model for achieving a switched region. It is also correct that most ad/ad regions occur at the boundaries of a switched region. One way to account for these data is if the initial event is a regional switch from ad/ab to ab/ad, and then (step two) for there to be a lateral signal where adaxial identity is propagated. The result would be ad/ad borders around the switched region. If these borders extend and run-together, a homogenous region of ad/ad leaf might occur indirectly (see Acknowledgements). Indeed, the signaling details that cause the switch in dorsoventrality are unknown.
If location is an indicator of function, the YABBY genes are like ROLLED1. The expression of YABBY genes in Arabidopsis is polarized to the abaxial half of the lateral organ (Siegfried et al., 1999). Ectopic expression phenotypes of Filamentous Flower (Fil) and Yabby3 (Yab3) confer abaxial cell identities onto adaxial surfaces of leaves (Siegfried et al., 1999
). Mutants in yab3 and fil that reduce or eliminate function respectively, have no phenotype (Siegfried et al., 1999
; Sawa et al., 1999
; Chen et al., 1999
). However, the fil yab3 double mutant has a phenotype which has been interpreted as partial adaxialization of abaxial cell types (Siegfried et al., 1999
). This observation suggests that there is functional redundancy within this gene family. This double mutant phenotype resembles that of Rld1 mutants in its partial adaxialization of abaxial tissue. However, it is important to point out that the Rld1 mutants phenotype remains unique in being the only dorsoventral polarity mutant phenotype in which switch in the polarity of the tissue has been observed.
With the existing data on YABBY genes and Rld1, there is no obvious way to fit Rld1 into the Arabidopsis dorsoventrality network. However, we will speculate on a few possibilities. One explanation of Rld1dominant mutants is that they down-regulate more than one YABBY gene, either directly (e.g. at the transcription level) or indirectly. This speculation is attractive because dominant negative mutants have the ability to remove a family of gene products from a specific time and place in development. Alternatively, RLD1 function could be necessary for any YABBY function, either upstream or down, or in balances of YABBY function. Siegfried and others (Siegfried et al., 1999) proposed that relative expression patterns of abaxial and adaxial specific genes might be responsible for differentiation of epidermal identities. Our results prove that there is communication between the epidermal layers, but the mechanism remains to be determined. We should emphasize these ideas are just conjecture because they require a level of regulatory homology between maize (a monocot) and Arabidopsis (a dicot) for which there is no evidence.
Mutations in the rld1 gene, like mutations in most of the genes involved in establishing dorsoventral polarity in leaves and other lateral organs, do not result in a complete loss of polarity. Our results suggest that there might be some redundancy in the maintenance of dorsoventral polarity in maize. We have found a dominant mutant mapping to a new gene, Rolled leaf2 (Rld2), which specifies an indistinguishable phenotype from the Rld1.
Our model suggests wild-type RLD1 is an abaxial factor required for maintenance and perhaps reception or propagation of abaxial tissue identity. The Rolled leaf1 mutant is unique in uncovering a signal transduced across the transverse dimension of the leaf, which is responsible for maintaining dorsoventral polarity in the leaf. It is possible that rld1+ functions in a dorsoventral signaling pathway that operates within the leaf only. We conclude that RLD1 is a novel component of the DV patterning signal network.
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ACKNOWLEDGMENTS |
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REFERENCES |
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