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American Society of Plant Biologists KNAT1 and ERECTA Regulate Inflorescence Architecture in Arabidopsis
a Botany Department, University of Toronto, 1265 Military Trail, West Hill, Ontario M1C1A4, Canada 1 To whom correspondence should be addressed. E-mail riggs{at}utsc.utoronto.ca; fax 416-287-7642
Plant architecture is dictated by morphogenetic factors that specify the number and symmetry of lateral organs as well as their positions relative to the primary axis. Mutants defective in the patterning of leaves and floral organs have provided new insights on the signaling pathways involved, but there is comparatively little information regarding aspects of the patterning of stems, which play a dominant role in architecture. To this end, we have characterized five alleles of the brevipedicellus mutant of Arabidopsis, which exhibits reduced internode and pedicel lengths, bends at nodes, and downward-oriented flowers and siliques. Bends in stems correlate with a loss of chlorenchyma tissue at the node adjacent to lateral organs and in the abaxial regions of pedicels. A stripe of achlorophyllous tissue extends basipetally from each node and is positioned over the vasculature that services the corresponding lateral organ. Map-based cloning and complementation studies revealed that a null mutation in the KNAT1 homeobox gene is responsible for these pleiotropic phenotypes. Our observation that wild-type Arabidopsis plants also downregulate chlorenchyma development adjacent to lateral organs leads us to propose that KNAT1 and ERECTA are required to restrict the action of an asymmetrically localized, vasculature-associated chlorenchyma repressor at the nodes. Our data indicate that it is feasible to alter the architecture of ornamental and crop plants by manipulating these genetically defined pathways.
The generation of asymmetries is an underlying theme in the development of higher eukaryotes. Organismal complexity arises progressively through the deposition and interpretation of positional information that refines and elaborates previously established spatial and temporal patterns. In plants, shoot and inflorescence development can be visualized as a reiterative process generating successively greater numbers of leaves, axillary meristems, and stems. The establishment and maintenance of this pattern requires the action of molecular switches that respond to positional information and mediate sharp transitions between different types of tissue and cellular identities. Loss of patterning factors in mutants can result in the transformation of cellular and tissue identities of one region to those characteristic of other locations, thus producing morphological novelties (Bowman, 2000  ; Ng and Yanofsky, 2001).
In higher plants, the formation of aerial organs is dependent on the activity of the shoot apical meristem (SAM), a dome-shaped morphogenetic field in which organ primordia are initiated. The SAM is divided into a central zone of undifferentiated initial cells, a peripheral zone in which lateral organs are initiated, and a basal rib zone in which stem tissue is specified. The SAM thus exhibits radial and apical-basal polarity as well as heterogeneity around its circumference. These asymmetries are necessary for proper SAM functioning and continued organ initiation throughout the life of the plant, but they also may contribute more directly to organ development by regulating patterns of shoot morphogenesis and differentiation. For example, during vegetative development, leaves are initiated at the peripheral zone of the SAM and undergo morphogenesis and differentiation so that, in most species, the adaxial (dorsal) and abaxial (ventral) sides of the leaf adopt distinct features (for review, see Bowman, 2000 Superimposed on the radial pattern of shoots are variations in tissue characteristics around the SAM's circumference, which are reflected in the incorporation of subsets of peripheral zone cells into organ primordia. Most commonly, primordia are initiated in succession at the SAM so that mature organs are arranged around the stem in a spiral phyllotaxy. In many upright plants, lateral organ elaboration is accompanied by the elongation of stem tissue to form internodes that punctuate stem–lateral organ junctions (nodes) along the vertical axis. In contrast to the nodes, which in plants with a spiral phyllotaxy exhibit obvious circumferential asymmetries, internodes appear radialized. It is not known how the heterogeneous circumferential pattern of the SAM is altered to produce seemingly radialized internodes.
Studies of the genetic control of stem development have focused on internode elongation. Arabidopsis mutants with reduced internode lengths include erecta (er), acaulis, brevipedicellus (bp), and gibberellic acid auxotrophs (Koornneef et al., 1983
In rice, a number of mutants have been characterized and grouped on the basis of the elongation pattern of the upper four or five internodes. One of these mutants exhibited shortened internodes and altered patterns of epidermal and subepidermal cell differentiation as a result of a loss-of-function mutation in the OSH15 KNOTTED-like homeobox (KNOX) gene (Sato et al., 1999
Through loss- and gain-of-function studies, class I KNOX genes have been implicated as regulators of meristem function in both monocots and dicots (Reiser et al., 2000 We are interested in the molecular mechanisms that dictate the architecture of higher plants. We investigated the mechanisms underlying stem morphogenesis by characterizing the bp mutant of Arabidopsis. We found that the bp phenotype is caused by a loss-of-function mutation in the class I KNOX gene KNAT1, and we provide evidence that KNAT1 functions along with ERECTA to radialize internodes and pedicels during stem elongation.
The BP Gene Promotes Cell Division and Elongation in Internodes During Arabidopsis vegetative development, leaves are formed in the absence of internode elongation, resulting in a rosette. The perception of floral inductive cues represses leaf development, initiates floral primordia outgrowth at the SAM, and induces elongation of stem tissue to form internodes. During floral morphogenesis, the determinate floral meristem gives rise to a conserved number and pattern of organs, whereas the basal portion of the primordium elongates to form the pedicel, the short stalk connecting the flower to the inflorescence stem. We have examined five independent alleles of the developmental form mutant bp. The original ethyl methanesulfonate–induced bp mutant (Koornneef et al., 1983 ) we have termed bp-1, and additional alleles were termed bp-2 through bp-5. In bp mutants, both internodes and pedicels are reduced in length and stem tissue develops bends that significantly alter shoot architecture. Pedicels bend downward so that the orientation of flowers and siliques is reversed relative to the wild type, and bends develop in inflorescence stems at leaf and floral nodes (Figure 1, Table 1). In the inflorescence stem, lateral organs always are elaborated on the concave side of the bend, and stripes of achlorophyllous tissue, initiated below the nodes, spiral down the stem (Figures 1C and 1D).
Morphometric analyses revealed that bp plants are significantly shorter than wild-type (Landsberg erecta [Ler]) plants, which could be attributable to a defect in internodal cell division, cell elongation, or both. To distinguish between these possibilities, we compared the epidermal cell lengths of bp internodes with those of Ler. We observed that Ler cells have an average length of 291 µm, whereas bp cells average 249 µm, or 86% of the wild-type length (data not shown). Taking into account the morphometric data (Table 1), it is apparent that there is both a cell expansion defect and a cell division defect in the mutant. However, not all cells are affected. Cells of the elongating stems and pedicels are most susceptible, whereas there are no obvious differences in leaf shape or size or in floral organ size or morphology.
Chlorenchyma Density Is Reduced Adjacent to Wild-Type Lateral Organs
In contrast to internodes and pedicels, all tissues are radially asymmetric at Lan nodes because of anatomical changes associated with the branching of lateral organs (Figure 2B). Most obvious is the absence of a discrete vascular bundle in the stem adjacent to the region of attachment of the lateral organ. This gap is formed as a result of the subnodal branching of a main stem bundle into the lateral organ to facilitate the exchange of water, metabolites, and signaling molecules between the organ and the rest of the plant. We also have found that the continuous distribution of chlorenchyma tissue in cortical regions of the internode is interrupted adjacent to lateral organs at the nodes, producing a collar of achlorophyllous tissue (Figure 2B). This perturbation in chloroplast density extends longitudinally to the top of the node, where a gap in the chlorenchyma distribution is apparent directly above the lateral organs (Figure 2C). The achlorophyllous cortex extends <100 µm above the node, past which the internode assumes its characteristic chlorenchyma radial pattern. These data indicate that the downregulation of chlorenchyma development occurs adjacent to lateral organs in wild-type Arabidopsis plants. The ERECTA gene influences multiple processes during Arabidopsis development, including internode and pedicel elongation and leaf and silique morphogenesis. Stem tissue thickness is increased in Ler plants, resulting in a more erect, rigid appearance. In general, we have found that increases in Ler stem thickness correlate with the enhanced development of supporting schlerenchyma tissue in internodes and pedicels (Figures 2D and 2E). Hand sections through Ler nodes also have revealed that the chlorenchyma downregulation observed adjacent to and above Lan lateral organs is expanded in Ler to include stem regions at the bases of leaves and flowers, implicating a role for ER in regulating chlorenchyma tissue development (Figure 2F).
bp Internodes Form Chlorenchyma-Deficient Stripes That Extend Basipetally from Nodes
In the epidermis, loss of stomata results in the alignment of epidermal cells into discrete files, which can be visualized using scanning electron microscopy on internode and pedicel surfaces (Figures 3H and 3I). In contrast, the abaxial side of Ler pedicels shows no evidence of a stripe (Figure 3J). Scanning electron microscopy confirmed that stripes initiate below the lateral organs along the inflorescence stem and extend proximodistally on the abaxial side of the pedicel. Occasionally, stripes extend beyond a single internode's length, resulting in two or more stripes on the same internode (Figures 1C, 1D, and 3B). Therefore, our microscopy data link anatomical defects with the morphological abnormalities that characterize bp. Specifically, bp internodes and pedicels lack cortical and epidermal radial symmetry on the abaxial region of pedicels and in internodes below the lateral organs. Furthermore, the similarity between the stripes of achlorophyllous tissue in bp internodes and pedicels and the wild-type nodal chlorenchyma distribution suggests that bp anatomical abnormalities may be patterned through the action of mechanisms at work during normal nodal development.
bp Stripes Are Associated with the Vasculature
A Functional ERECTA Gene Suppresses the bp Phenotype Because the bp mutation is in an erecta background and the ERECTA gene influences stem elongation and nodal chlorenchyma patterning, we crossed bp with Lan to observe the single mutant bp/ER phenotype. These plants were shorter than Lan plants, pedicels were reduced in length, and siliques were oriented approximately perpendicular to the inflorescence axis (Figure 3K, Table 1). In addition, more subtle bends were observed in the inflorescence stem at the nodes. Although sections through bp/ER pedicels revealed achlorophyllous abaxial and lateral regions, no stripe was evident in bp/ER pedicels (Figures 3L and 3M). In the inflorescence stem, a stripe was present in bp/ER internodes beneath lateral organs, but it did not extend as far down the stem as in bp plants (data not shown). These results indicate that the BP and ER genes have overlapping roles in regulating plant architecture and chlorenchyma differentiation in stem tissue. In summary, bp morphological defects correlate with abnormal patterns of tissue differentiation in internodes and pedicels. The similarity of chlorenchyma patterning in bp internodes and pedicels to wild-type nodal asymmetries, combined with the association of vasculature and stripes with common lateral organs, suggests that altered internode and pedicel patterns of differentiation in bp may be extensions of wild-type nodal characteristics. Furthermore, these results demonstrate that the ER gene functions redundantly with BP to influence plant architecture and stem differentiation.
The bp (Ler) Phenotype Is Caused by a Mutation in the Class 1 Homeobox Gene KNAT1
BP Expression Domains Previous studies have shown that BP is expressed during inflorescence development in internodes, pedicels, and carpels (Lincoln et al., 1994 ). We have investigated its expression pattern further using in situ hybridization and  -gluc-uronidase (GUS) staining of transgenic plants harboring a BP::GUS reporter gene construct. Figure 6A shows that the gene is turned on initially at the late globular stage of embryo development in presumptive hypocotyl tissue. Expression persists in the hypocotyl throughout the heart and torpedo stages (Figures 6B and 6C) and into the vegetative stage (data not shown). At later embryonic stages and throughout vegetative development, BP is turned on below developing leaf primordia at the shoot apex (Figure 6D). During inflorescence development, BP is expressed in pedicels and internodes in cortical tissues (Figures 6E and 6F). During floral development, expression is restricted to the marginal domains of carpels, with no expression in the outer three whorls (Figure 6G). Despite strong expression of BP in the hypocotyl and carpels, no obvious defects were observed in these tissues in the bp mutant, suggesting that redundant factors compensate for the loss of BP.
Reduced Meristem Function Is Not Evident in bp On the basis of domains of BP expression and its role in meristem function, as ascribed in gain-of-function studies (Lincoln et al., 1994 ; Chuck et al., 1996), we wished to establish whether meristem function is affected in bp mutants. We observed no decrease in the number of lateral organs initiated by either the vegetative or inflorescence SAM during bp development (data not shown). However, bp initiates leaves at a slightly faster rate than does Ler, and it also flowers slightly earlier (data not shown). This indicates a role for BP in the vegetative SAM as a regulator of rates of leaf initiation and floral transition, but not of meristem activity per se.
Recently, Pautot et al. (2001)
Finally, we examined the genetic relationship between BP and ASYMMETRIC LEAVES2 (AS2) during leaf development. as2 leaves show lobes and the occasional production of ectopic meristems on adaxial surfaces. These phenotypes are consistent with an increase in meristematic identity in the leaf, which is supported by the ectopic expression of KNOX genes in as leaf tissue (Byrne et al., 2000
Collectively, these results indicate that although BP's expression domain and gain-of-function phenotypes implicate a meristematic role (Lincoln et al., 1994
Stems of higher plants offer support to the aerial portion of the plant body and serve as conduits for the transport of water and metabolites between roots and leaves. Despite the critical roles played by stems, very little is known about the underlying molecular mechanisms governing their development and morphology. As a first step toward understanding the genetic basis of stem development, we have characterized the bp mutant of Arabidopsis, which exhibits bends in inflorescence stems and pedicels as well as reductions in their lengths. Our studies indicate that loss-of-function mutations in both the BP and ERECTA genes are required to give rise to the bp phenotype. These data demonstrate a previously unknown link between KNOX gene activity and dicot stem development and raise questions regarding the possible role of meristem-regulating factors during organogenesis.
The Function of BP and ER during Stem Development In the bp mutant, cortical and epidermal tissues of internodes acquire asymmetric patterns of cell differentiation, giving rise to visible stripes of tissue. On the basis of four observations, we propose that these asymmetries are related to the wild-type nodal anatomy. First, Lan nodes exhibit asymmetries in chlorenchyma patterning in lateral regions that appear identical to bp stripes in transverse sections. Second, the erecta mutation results in reduced density of chlorenchyma distribution below the lateral organs and enhancement of the bp stripe phenotype. Third, the wild-type achlorophyllous domains above and around the bases of lateral organs are enhanced in bp mutants. Fourth, the bp stripe initiates directly beneath the lateral organs, where Ler chlorenchyma density is reduced, and is linked to the vascular bundle that services the lateral organ. The bp internodal stripe, therefore, seems to represent a shift of wild-type nodal asymmetries into internodes, implicating the BP and ER genes in the regulation of internodal symmetry. The enhancement of wild-type nodal asymmetries in bp, combined with the normal development of chlorenchyma in nonstripe regions, implies that asymmetries in wild-type and mutant stem cortices are caused by the action of a repressor of chlorenchyma development. The influence of this factor may not be confined to chlorenchyma repression, because it also could function to regulate other aspects of nodal differentiation and morphogenesis (e.g., maintenance of active mitosis). The localization of repressor activity adjacent to lateral organs suggests that its function is linked to asymmetries associated with organ initiation in the peripheral zone. We speculate that BP and ER act to restrict the domain of action of the repressor such that in their absence wild-type chlorenchyma asymmetries are enhanced and internode differentiation is altered. An asymmetric increase in the level of such a repressor at the node, next to the lateral organ, may induce sufficient polarity to induce bending in stems.
The link between the bp stripe and the vasculature provides evidence that the nodal repressor of chlorenchyma development is related to the vasculature. Our data are consistent with the flux of repressor basipetally from the node through the vasculature to alter differentiation in overlying tissue layers. However, we cannot exclude the possibility that the repressor has independent functions in both positioning vascular bundles and effecting cortical and epidermal differentiation in internodes. The action of the repressor in bp stems reveals that mutant internodes develop as mosaics, with individual sectors represented by a vascular bundle and overlying cortex and epidermis. At a given transection along an internode, units differ in the concentration of repressor with which they are or have been associated. In the wild type, therefore, repression of the action of this "asymmetrizing" molecule by BP and ER leads indirectly to a normalization of unit identities in internodes, which underlies the switch between asymmetric nodal organization and radialized internodes. Supporting evidence for a link between the bp stripe and the vasculature comes from other studies examining KNOX gene function. For example, in the maize knotted1 mutant, leaf blade cells over veins differentiate into sheath-like cells as a result of the misexpression of KNOTTED1 (Smith et al., 1992
Pedicel Dorsoventrality Is Specified by BP
The first of these is radial polarities inherent to the inflorescence axis. Recently, the relative proximity of primordial adaxial and abaxial leaf domains to the center of the shoot axis was suggested to underlie the development of leaf dorsoventrality (McConnell et al., 2001 The second mechanism underpinning dorsoventral pedicel asymmetries in bp may relate to asymmetry in pedicel vasculature patterning. We have observed that adaxial vascular bundles usually are much smaller and less distinct than those in abaxial regions. This property probably is related to the branching of vasculature into lateral organs from positions below the node. If the chlorenchyma repressor acts in a vasculature-dependent manner in pedicels as well as internodes, then dorsoventral vasculature patterning asymmetries could underlie adaxial–abaxial differences in bp pedicel histologies. In either situation, it appears that the concentration of repressor action on the abaxial sides of pedicels induces sufficient polarity for downward bends to develop in the bp mutant. It is unclear how the receptor kinase encoded by ERECTA, and a putative transcription factor encoded by BP, are engaged in regulating stem architecture. To identify the molecules involved in this pathway(s), we are now using microarray analyses to identify other genes regulated by BP and are characterizing suppressor mutants of bp in which its defects are ameliorated.
BP and Meristem Function
During evolution, meristem-associated factors such as BP may have acquired a role in controlling the development of nonmeristematic tissues such as internodes. Notably, loss-of-function mutations in the rice class I KNOX gene OSH15 also give rise to defects during stem development (Sato et al., 1999
Plant and Genetic Materials Seed of Arabidopsis thaliana, ecotype Landsberg erecta (Ler), were used for most experiments reported. Fast neutron–mutated Ler M2 seed were purchased from Lehle Seeds (Round Rock, TX). Seed of the mapping mutant brevipedicellus (bp), Landsberg seed wild type for the ERECTA gene (Lan), bacterial artificial chromosome clones, ap2-5 mutant seed, and as2-1 mutant seed were obtained from ABRC (Ohio State University, Columbus). Plants were grown indoors under constant illumination with fluorescent bulbs. Additional mutant lines were provided by Drs. Camille Steber (Washington State University, Pullman), Allen Sessions (University of California, San Diego), Matt Metz (University of California, Berkeley), and Naomi Ori (Plant Gene Expression Center, Albany, CA). The BP:: -glucuronidase (GUS) transgenic line was provided by Sarah Hake and described by Ori et al. (2000). Crosses between bp-2 and ap2-5 and between bp-2 and as2-1 were generated and confirmed as double mutants by morphological criteria.
Mapping of the bp Mutation and Mutant Rescue
Molecular mapping and subsequent DNA gel blot analyses suggested that the KNAT1 gene may be responsible for the bp phenotype. We amplified a 4.7-kb fragment from genomic DNA using the primers 5'-GGACTAGTTTCGGTCTAGTGCAGTGATGAGG-3' and 5'-TGGTCGACTGTCCGCATCAGATGACGAGTG-3'. This strategy introduced SpeI and SalI sites at the ends, and after SpeI–SalI digestion, the fragment was mobilized into pGVPT-HPT (Becker et al., 1992
Tissue Preparation for Light Microscopy/Cell Length Measurements To examine the morphology of tissue sections, 2-mm tissue segments were fixed in cold FAA (50 mL of 95% ethanol, 5 mL of glacial acetic acid, 10 mL of 37% formaldehyde, and 35 mL of distilled water) for a minimum of 48 hr and stored in FAA at 4°C. Tissue was washed in 70% ethanol and double distilled water before secondary fixation in 1% aqueous osmium tetroxide at room temperature for 2 hr. After distilled water washes, tissue was dehydrated in an acetone series and infiltrated and embedded in Spurr's low-viscosity resin. Sections (1.5 µm thick) were cut using glass knives and an ultramicrotome. Sections were stained with 0.05% toluidine blue in 0.05% aqueous borax and mounted in Cytoseal 60 (Stephens Scientific, Riverdale, NJ). Images were captured with a Zeiss (Jena, Germany) Axiophot photomicroscope.
Scanning Electron Microscopy
Hand Sectioning of Stems and Pedicels
In Situ Hybridization and GUS Histochemical Assays
The authors thank Sarah Hake, Rob Martienssen, Mary Byrne, Matt Metz, and Camille Steber for sharing materials and information. We also are indebted to John Tang, Raymond Orr, Barbara Ambrose, Bob Schmidt, Marty Yanofsky, Medard Ng, Dino Balkos, and Thomas Berleth for assistance with techniques and their advice about this project. We appreciate the helpful comments of two anonymous reviewers. We acknowledge ABRC for providing seed and bacterial artificial chromosome clones and Nancy Dengler and Clare Hasenkampf for sharing equipment and for valuable comments on the manuscript. We thank Annette Rzepczyk for excellent technical assistance. S.J.D. was supported by a postgraduate fellowship from the Natural Sciences and Engineering Research Council of Canada (NSERC) and a traveling fellowship from The Company of Biologists, Ltd. G.C. was supported by a University of California fellowship (to Sarah Hake). This research was supported by a grant from NSERC to C.D.R.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010391. Received September 6, 2001; accepted November 16, 2001.
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INTRODUCTION
200 kb, all of which had been sequenced completely by the Arabidopsis Genome Initiative (2000)
