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First published online December 17, 2004; 10.1105/tpc.104.026898 © 2005 American Society of Plant Biologists Asymmetric Auxin Response Precedes Asymmetric Growth and Differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis LeavesDepartment of Biological Sciences, University of Lethbridge, Lethbridge, Alberta, TIK 3M4, Canada 1 To whom correspondence should be addressed. E-mail schultz{at}uleth.ca; fax 403-329-2242.
We have analyzed the development of leaf shape and vascular pattern in leaves mutant for ASYMMETRIC LEAVES1 (AS1) or AS2 and compared the timing of developmental landmarks to cellular response to auxin, as measured by expression of the DR5:ß-glucuronidase (GUS) transgene and to cell division, as measured by expression of the cycB1:GUS transgene. We found that the earliest visible defect in both as1 and as2 first leaves is the asymmetric placement of auxin response at the distal leaf tip. This precedes visible changes in leaf morphology, asymmetric placement of the distal margin gap, formation of margin gaps along the leaf border, asymmetric distribution of marginal auxin, and asymmetry in cell division patterns. Moreover, treatment of developing leaves with either exogenous auxin or an auxin transport inhibitor eliminates asymmetric auxin response and subsequent asymmetric leaf development. We propose that the initial asymmetric placement of auxin at the leaf tip gives rise to later asymmetries in the internal auxin sources, which subsequently result in asymmetrical cell differentiation and division patterns.
Growth and development of the plant shoot requires that a group of indeterminate stem cells, the shoot apical meristem (SAM), continuously replenishes itself and produces determinate lateral organs from its flanks. The SAM is radially symmetrical, and lateral organs are produced from it in a regular pattern. The maintenance of SAM symmetry and formation of organs require integration and coordination of processes controlling cell growth and cell division in diverse tissue types. Asymmetric growth of the shoot does occur in response to either light or gravity. Both gravitropism and phototropism are regulated through asymmetric distribution of the hormone auxin, with both environmental stimuli proposed to cause an altered distribution of auxin carrier proteins in the plasma membrane (Friml, 2003  ).
Lateral organs produced from the SAM, such as leaves, usually attain both adaxial–abaxial and proximodistal asymmetry. A large set of genes, isolated from a range of angiosperm species, has been implicated in the specification of leaf adaxial–abaxial asymmetry. In Arabidopsis thaliana, mutations in the genes PHABULOSA (PHB), FILAMENTOUS FLOWER (FIL), PINHEAD/ZWILLE, ARGONAUTE1 (AGO1), GYMNOS, CRABS CLAW, ETTIN, YABBY2, KANADI (KAN), ASYMMETRIC LEAVES2 (AS2), and AS1 result in aberrant adaxial–abaxial specification of foliar organs (Bohmert et al., 1998
Specification of proximodistal asymmetry is less well characterized, although AS1 and AS2 in Arabidopsis and orthologs ROUGH SHEATH2 (RS2) in maize (Zea mays) and PHAN in Antirrhinum seem to play a direct or indirect role. Mutations in rs2 show defects in proximodistal specification, with blade cells adopting a sheath-like identity (Schneeberger et al., 1998
Plant growth regulators also seem to play a role in the establishment of the indeterminant versus determinant pathways and hence may act to establish proximal/distal asymmetries. Cytokinin induces expression of STM and KNAT1 (Rupp et al., 1999
Although each leaf displays proximodistal and adaxial–abaxial polarity, the expansion of the leaf blade, position of leaf serrations, and loops of vascular tissue create an essentially bilaterally symmetrical organ across the midvein. Moreover, changes in leaf shape are coupled with changes to vascular pattern, suggesting a link between the controls on cell growth, division, and differentiation (Dengler and Kang, 2001
Complementation Tests Mutants having leaf shape abnormalities were assessed for defective margins. Eight mutants having asymmetric or lobed leaves were found to have margin gaps and were tested for allelism to as1-1 and as2-1 by intercrossing (Table 1). Five new alleles of AS1 were identified (CS444, CS3240, CS3250, GW4-0-0, and AW179, designated as1-15, as1-16, as1-17, as1-18, and as1-19, respectively) and two new alleles of AS2 (CS230 and CS3381, designated as2-6 and as2-7, respectively). Preliminary examination of plants homozygous for the new AS1 alleles indicated that their phenotypes were not distinct from previously described alleles. Therefore, we choose alleles as1-1 and as1-16 from Landsberg erecta (Ler) and Columbia (Col) ecotypes, respectively, for further analysis. Plants homozygous for as2-7 have a phenotype somewhat different from other as2 alleles; therefore, we choose plants homozygous for as2-7 (Col background) as well as for as2-1 (Ler background) for further analysis.
as1 and as2 Leaf Shape First and fifth leaves of both as1 and as2 plants are obviously distinct from the wild type in shape and size, generally having smaller, more curled, and heart-shaped blades, shorter petioles from which asymmetric lobes emerge, and protrusions from the leaf blade that are larger and asymmetrically placed compared with wild-type serrations (Table 2). When seedlings are dissected to expose the SAM and young leaf primordia, no differences are evident in the size, shape, or spacing of the first two primordia in mutant plants compared with the wild type up to 5 d after germination (DAG; where transfer to growth chamber is 0 DAG) or for the fifth primordium up to 10 DAG (data not shown). By 6 DAG for the mutant first leaf and by 11 DAG for the fifth, both shape and cell differentiation are noticeably different than the wild type (Figures 1D, 1E, 1G, 1H, 2E, 2F, 2I, and 2J). Leaf primordia of both as1 and as2 plants curl inward, are smaller than wild-type leaves, wider at the distal than the proximal end of the blade, and show little petiole development. Moreover, some asymmetric protrusions are evident at the base of the leaf. At this stage, differentiation of margin cell files begins in the wild type, first visible adjacent to the distal leaf tip as two to three files of slightly larger and more elongate cells than the cells on either the adaxial or abaxial blade surface (Figures 1A, 1B, 2A, and 2B) and progressing proximally. Cells at the distal primordial tip remain small and unelongated and often include a large number of stomata and/or trichomes and associated basal cells (Figures 1A and 1B). We term this region the distal margin gap. In as1 and as2 leaves at this stage, margin cells are smaller and less elongated than in the wild type (Figures 1D, 1E, 1G, 1H, 2E, 2F, 2I, and 2J), and the distal margin gap is sometimes asymmetrically positioned at the leaf tip (Figures 1D, 2F, and 2I).
Because of the proposed relationship amongst the leaf margin, leaf expansion, and abaxial/adaxial specification (Waites and Hudson, 1995 ; Ori et al., 2000), we assessed the integrity of the margin by examining mature leaf segments of as1 and as2 first and fifth leaves by SEM and in all found disruptions (Figures 1F, 1I, 2G, 2H, 2K, and 2L). In wild-type leaves (Col and Ler ecotypes), the margin consists of two to six files of linear and elongated cells that span the leaf edge at the abaxial/adaxial boundary (Figures 1C, 2C, and 2D). In first leaves, the margin is continuous except for the distal margin gap. In fifth leaves, the distal margin gap is also present (Figures 2A and 2B), and a margin gap involving a similar number of cells also occurs infrequently at the tips of leaf serrations (one gap observed in four leaves, Figure 2D). In all of as1 and as2 first leaves, margin gaps are seen in variable positions within the proximal half of the leaf and contain cell types similar to those seen on the abaxial leaf surface, often interspersed with stomata (Figures 1F and 1I). as1 and as2 fifth leaves show as many as four margin gaps per leaf (Figures 2G, 2H, 2K, and 2L). In as1 mutants, margin gaps are most common in the proximal portion of the leaf (as1-1, 86%, n = 14; as1-16, 85%, n = 13), whereas in as2 mutants, they are observed exclusively in the proximal portion of the leaf. Because such gaps have been found associated with lobe sinuses in other alleles (Ori et al., 2000), we assessed the position of margin gaps relative to lobes (Table 3). In all alleles except as1-1, gaps are most common at the lobe tip. Other differences in as1 and as2 margins compared with the wild type include margin cells that are not positioned at the leaf edge but rather are found adjacent to the margin in place of laminar epidermal cells and variable numbers of margin cell files, such that, in places, the margin consists of as many as 15 cell files (data not shown).
We looked at the patterns of cell division in the wild type, as1-16, and as2-1 first leaves using the cycB1:ß-glucuronidase (GUS) reporter construct (Doerner et al., 1996 ) and found differences in the patterns of cell division in mutant leaves (Table 4, Figure 3). At 4 DAG, cycB1:GUS expression is similar in distal and proximal leaf halves and shows no significant difference between the wild type and as1-16 (Table 4, Figures 3A and 3D), but the number of cells expressing the reporter gene is reduced in both halves of as2-1 leaves (Table 4, Figure 3G). Consistent with basipetal decrease in cell division (Donnelly et al., 1999), at 5 DAG, cycB1:GUS expression is diminishing in the distal half of both wild-type and mutant leaves, and the number of cells expressing is again lower in as2-1 (Table 4, Figures 3B, 3E, and 3H). At 7 DAG, cycB1:GUS expression is virtually absent in the distal half of all leaves (Table 4, Figures 3C, 3F, and 3I). We next assessed asymmetrical expression of cycB1:GUS by determining cell divisions in four sections of the leaf: left and right sides of the midvein within both distal and proximal halves. Based on the number of cell divisions in each side, left and right sides of distal and proximal halves were categorized as high or low, and the mean high versus mean low number of cell divisions was compared by Student's t test. At some stages, the comparison between high and low showed significant differences in the wild type, presumably because these stages had a low number of cell divisions and relatively high standard error. In these cases, we discounted similar differences in the mutants because they presumably would not contribute to asymmetry. Based on this analysis, mutants showed significant difference between high and low sides in the proximal half at 7 DAG (Figures 3F and 3I). Whereas in the wild type, the number of cells expressing GUS in the wild type low proximal side and the high proximal sides was not significantly different (27.8 ± 14.7 versus 33.6 ± 16.7), in both as1-16 and as2-1, this difference was significant (27.1 ± 14.2 versus 50.2 ± 17.8 and 12.0 ± 8.0 versus 17.2 ± 9.2, respectively). Thus, at 7 DAG, the proximal half of mutant leaves shows distinct asymmetry in the number of dividing cells, consistent with the asymmetrical leaf lobes within the proximal leaf blade observed at leaf maturity.
as1 and as2 Venation Pattern As described by other studies (Semiarti et al., 2001 ), venation pattern is simpler through the as1 and as2 leaf blades but shows increased numbers of veins within the petiole (Table 5). It is possible that the simplicity of the vascular pattern indicates delayed vascular development in as1 and as2 leaves, such that full maturity is never reached. In fact, although landmarks of vascular differentiation are reached somewhat later than in the wild type (Table 4), all events seem to occur, indicating that the as1 and as2 leaves are fully mature.
To determine if the sequence and direction of vascular pattern formation was similar to the wild type, we examined development of vascular pattern in as1 and as2 first leaves (Table 4, Figure 4). The differentiating midvein in mutant first leaves was visible in essentially the normal position and normal acropetal direction, although it occurred slightly later (6 DAG) than in the wild type (5 DAG; Figure 4A). Moreover, midvein differentiation frequently terminated before the leaf apex or veered away from the leaf tip (Figures 4E and 4G). As in the wild type, distal secondary veins were initiated at the apical end of the midvein (Figures 4A and 4D), although more frequently than in the wild type, one secondary vein was initiated later than the other or was initiated below the distal tip of the midvein (Figures 4E and 4G). The aberrant differentiation of the midvein and asymmetric initiation of secondary veins often correlated with an asymmetrically placed margin gap. The distal secondary veins rejoined the midvein at a more proximal point of the midvein than in the wild type, resulting in larger distal secondary loops (Figures 4E, 4F, 4H, and 4I). These large loops were often divided by subsequent intercalary formation of secondary veins (Figures 4E, 4F, 4H, and 4I). Differentiation of secondary veins, as indicated by xylem thickenings, occurred basipetally in both the wild type and mutants (Figures 4B, 4E, and 4H). Initiation of proximal secondary veins, which occurs from the distal secondaries at about the midpoint of the leaf blade in the wild type (Figures 4B and 4C), occurs at a more distal point in the mutant leaves (Figures 4E, 4F, 4H, and 4I).
Auxin Response in as1 and as2 Leaves Reasoning that the altered venation pattern in as1 and as2 might be predicted by an altered auxin response pattern, we crossed DR5:GUS into the as1-16 and as2-1 background. The DR5:GUS construct links the reporter gene to a synthetic auxin inducible enhancer, so that reporter gene expression is an indicator of high auxin response (Ulmasov et al., 1997 ). In wild-type first leaves, DR5:GUS appears 3 DAG in a single cell at the leaf distal tip (Table 4, Figure 5A). In mutant first leaves, DR5:GUS is evident with similar timing. However, the position is often asymmetric relative to the leaf, shifted to one side of the distal tip (Table 4, Figures 5B and 5C). Subsequent DR5:GUS expression in mutant leaf blades is slightly later than in the wild type (Table 4), and no differences in pattern are evident, although expression within the blade at these stages is very transient, so that pattern differences would be difficult to detect (Figures 5D to 5F). At this stage, distal tip expression coincides with the distal margin gap, and in mutant leaves, both sometimes appear asymmetrically placed (Figure 5E). Asymmetric DR5:GUS expression is especially evident when expression begins in hydathodes (Table 4). In wild-type first leaves, hydathode expression usually appears in two points at equivalent positions along the leaf margin (Figure 5G). By contrast, expression in both as1-16 and as2-1 may begin at just one point and be followed by expression in another one or two, often unequally positioned points in as2-1 leaves (Figures 5H and 5I). Expression of DR5:GUS at this stage coincides with margin gaps (Figures 5J to 5L), and the margin gaps seem to contain more cells in the mutants than the wild type (cf. Figures 5K and 5L to 5J).
Response of as1 and as2 Phenotypes to Exogenous Auxin and Auxin Transport Inhibitor The correlation of early asymmetric auxin response with later asymmetric leaf morphology suggests that altered leaf morphology may result from altered auxin response. If this notion is correct, one might expect that altering auxin response in mutant leaves could alter the mutant phenotype. We therefore treated developing wild-type and mutant leaves with either the synthetic auxin 2,4-D or the auxin transport inhibitor naphthylphthalamic acid (NPA; Sigma-Aldrich). We then compared the pattern of auxin response (DR5:GUS expression), leaf shape, and leaf venation in developing mutant and wild-type leaves (Figure 6, data not shown for as2-1). Treatment of developing mutant and wild-type leaves with 10–7 M 2,4-D results in an auxin response that appears somewhat more intense and more widespread than in untreated leaves (cf. Figures 6A to 6H with 5A to 5L). Nevertheless, the mature leaf shape and vascular pattern of treated leaves (Figures 6D and 6H) appears unchanged compared with untreated leaves. By contrast, treatment with 10–6 M 2,4-D, 10 µM NPA, or 30 µM NPA results in drastically altered auxin response and leaf development in both wild-type and mutant leaves such that mutant leaves are indistinguishable from the wild type. In both mutant and wild-type leaves treated with 10–6 M 2,4-D, the distal tip auxin maximum is visible slightly later and initially occupies several cells (Figures 6I and 6M) rather than the single cell typical of untreated leaves (Figures 5A and 5B). By 5 DAG, expression increases to occupy approximately half the developing primordium (Figures 6J and 6N). The increased size of the distal maximum makes it difficult to compare the symmetry to that in untreated leaves; however, we are unable to detect any difference in position of the larger distal maximum in the treated wild type compared with treated mutants. Moreover, in contrast with untreated leaves, no vascular differentiation is visible by 6 DAG in treated leaves (Figures 6K and 6O), and by 10 DAG treated leaves usually remain small with little midvein differentiation (Figures 6L and 6P). Similarly, mutant and wild-type leaves treated with 10 or 30 µM NPA were indistinguishable (data not shown for 30 µM). Initial expression of DR5:GUS in 4 DAG treated wild-type and mutant primordia show no clear distal maximum, but rather a less intense expression in several cells across the apex (Figures 6Q and 6U). Because of the variable number and position of cells showing DR5:GUS expression, we were unable to compare the symmetry to that in untreated leaves. However, there is no apparent difference in symmetric position of expressing cells in the treated wild type compared with treated mutant primordia. As development proceeds in both treated wild-type and mutant leaves, DR5:GUS is expressed in two loops of cells (Figures 6R, 6S, 6V, and 6W), the inner loop coinciding later with the formation of vascular tissue (Figures 6S and 6W). In contrast with untreated leaves, in NPA-treated wild-type and mutant leaves, DR5:GUS expression never resolves to the hydathodes, but rather is seen in a broad band of cells between the leaf margin and the vascular tissue (Figures 6S, 6T, 6W, and 6X). No differences in symmetry of leaf shape or vascular pattern are evident between wild-type and mutant leaves at 10 DAG; the only difference is a simpler venation pattern in mutant leaves (Figures 6T and 6X).
We have analyzed several defects in developing as1 and as2 leaves, including vascular pattern, leaf shape, leaf margin defects, cell division patterns, and auxin response. Early in development of wild-type leaves, an auxin response maximum is located symmetrically within the distal leaf tip. We found that the earliest visible defect in as1 and as2 leaves is the asymmetric placement of this auxin response maximum. Subsequent auxin response pattern is also asymmetric. Furthermore, cell division patterns are shown to be asymmetric in the mutants compared with the wild type. Finally, when a more symmetric auxin response is induced in mutant leaves through treatment with either exogenous auxin or auxin transport inhibitor, a more symmetric leaf morphology and venation pattern results. We suggest that the early, distal tip asymmetry may lead to subsequent asymmetries in the auxin response pattern and hence generate an asymmetric vein pattern. We further propose that the asymmetric auxin distribution in as1 and as2 leaves affects cell division patterns and hence generates asymmetric leaf shape. This suggests a mechanism whereby cell differentiation patterns, including vascular pattern, and cell divisions may be coordinated.
Asymmetric Auxin Response Predicts Asymmetric Vascular Pattern Altered placement of secondary veins in as1 and as2 leaves suggests that the second, marginal auxin source may be altered. However, changes in symmetry of auxin distribution from the marginal source to the leaf lamina are difficult to assess using DR5:GUS expression because auxin response is quite transient in cells that will become vascular tissue. Later in leaf development a less transient response to marginal auxin becomes concentrated to distinct points, the hydathodes, along the leaf margin. In wild-type leaves, there are usually two points symmetrically positioned along the leaf margin, whereas in as1-16 and as2-1 leaves, the number of points varies, and their position is often asymmetric. When wild-type or as leaves are treated with 2,4-D or NPA, both marginal and later hydathode DR5:GUS expression are altered to produce phenotypes indistinguishable from one another. Subsequently, symmetry of secondary and higher order vein patterns are also indistinguishable. Thus, our results suggest strong correlations firstly between asymmetries of different auxin responses and secondly between asymmetries of auxin response and vascular pattern. When the auxin response maxima resulting from both the primary, external auxin source is asymmetrically positioned, subsequent secondary, marginal sources are also asymmetrically positioned. Although it is possible that the two are independently controlled, we suggest that the first asymmetry results in the second. Such coordination would allow the generation of an integrated vascular pattern even if the distribution of auxin driving the pattern is altered.
Ectopic Expression of KNAT Genes Results in Aberrant Regulation of Growth Regulators
In this study, we have shown that leaves mutant for AS1 or AS2 also show altered positions of auxin response, suggesting either that the auxin source is altered or that auxin transport from source to sink is altered. Changes to the auxin source could result from as1 and as2 defects in the previously formed primordia (in the case of the first leaf, the cotyledons). Alternatively, changes in auxin transport could be the result of as1 and as2 induced changes within the leaf primordia, such as KNAT gene misexpression. Although we do not know how misexpression of KNAT genes might lead to altered auxin transport, one possibility is that downregulation of KNAT genes predisposes cells to transport auxin, such that ectopic KNAT expression disrupts routes of auxin transport. Consistent with this idea, downregulation of KN1 is a characteristic of vein initiation (Smith et al., 1992
Asymmetric Auxin Response Precedes Asymmetric Cell Division Patterns
Our data support the idea that symmetric response to auxin along the leaf margin is critical to symmetric cell division patterns and leaf expansion. Studies on leaf vascular pattern indicate that the leaf margin is a source of auxin (Mattsson et al., 1999 The pattern of response to auxin, which is initially transient throughout the margin and subsequently prolonged at defined points along the margin, suggests a possible mechanism whereby the marginal auxin and its symmetrical and basipetal response may be regulated. Margin cells differentiate first near the leaf apex, and subsequent differentiation is basipetal along the leaf circumference. If, once fully differentiated, margin cells no longer serve as a source of auxin, auxin response would diminish basipetally. This is consistent with both the basipetal reduction in cell division and the basipetal development of leaf vascular pattern, two processes proposed to occur in response to auxin.
Symmetrical Auxin Distribution Coordinates Symmetrical Cell Differentiation and Division Patterns
Plant Material and Growth Conditions Mutant lines cs146 (as1-1), cs444 (as1-14), cs3240 (as1-16), cs3250 (as1-17), cs3117 (as2-1), cs3118 (as2-1), cs230 (as2-13), and cs3381 (as2-14) were obtained from the Arabidopsis Biological Resource Centre (Columbus, OH); line GH4-0-0 is from an ethyl methanesulfonate–mutagenized Col-1 population obtained from G. Haughn (University of British Columbia); line AW179 is from a  -irradiated Ler population from A. Wilson (John Innes Centre). The cycB1:GUS line was kindly provided by P. Doerner (University of Edinburgh) and the DR5:GUS line by J. Murfett (University of Missouri, Columbia, MO). To generate AS1 and AS2 mutants expressing the cycB1:GUS or DR5:GUS fusion, as1-16 and as2-1 were crossed to the respective expression line. Plants showing the as mutant phenotype in the F2 populations were screened for cycB1:GUS expression in root tips or DR5:GUS expression in leaves. F3 seed was collected from those showing expression, and lines expressing GUS in all F3 plants were used for subsequent analysis. Plants for analysis of mature leaves were grown on soil, and seedlings for analysis of developing leaves were grown on media unsupplemented or supplemented with 10–6 M 2,4-D, 10–7 M 2,4-D, 10 µM NPA, or 30 µM NPA (Sigma-Aldrich, St. Louis, MO) as described by Steynen and Schultz (2003).
Microscopy and Analysis
Seed was kindly provided by Peter Doerner, George Haughn, Jane Murfet, Alison Wilson, and the Arabidopsis Biological Resource Centre. We thank John Bain, George Haughn, Shelley Hepworth, Ljerka Kunst, and members of the Schultz lab for insightful comments on the manuscript. This work was supported through Natural Sciences and Engineering Research Council of Canada Summer Undergraduate Research Awards to J.M.Z. and D.A.B. and a Natural Sciences and Engineering Research Council of Canada Operating Grant to E.A.S.
The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) is: Elizabeth A. Schultz (schultz{at}uleth.ca). Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.104.026898. Received August 24, 2004; accepted October 7, 2004.
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