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First published online January 19, 2005; 10.1105/tpc.104.028936 © 2005 American Society of Plant Biologists
The Role of KNOX Genes in the Evolution of Morphological Novelty in Streptocarpus
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
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; Sucena et al., 2003). Variation in the activity of transcription factor genes also underlies some of the artificially selected morphological changes that accompanied the domestication of maize (Zea mays) (Doebley et al., 1998; Doebley and Lukens, 1998; Wang et al., 1999). In contrast with closely related species, higher order taxa tend to differ more dramatically in body plan, for example, in the number, identity, or relative positions of organs. Such evolutionary innovations may have also involved transcription factor genes because the changes sometimes correlate with altered transcription factor expression and can be mimicked by mutations in transcription factor genes in both plants and animals (Doebley and Lukens, 1998; Carroll, 2000).
One genus of plants that encompasses species with different body plans is Streptocarpus, the Cape primrose. Streptocarpus consists of 
140 African and Madagascan species that fall into two main clades on the basis of internal transcribed spacer (ITS) sequence phylogenies and chromosome numbers, and are broadly consistent with classical taxonomic subdivisions (Hilliard and Burtt, 1971; Möller and Cronk, 2001). Clade I consists of caulescent species that form stems and leaves conventionally from a shoot apical meristem (SAM; Figure 1B). Clade I corresponds to subgenus Streptocarpella with the genus Saintpaulia (African violets) nested within it (Möller and Cronk, 1997). Like most Gesneriaceae, caulescent Streptocarpus species favor warm, humid, and aseasonal habitats (Burtt, 1998). Clade II species, corresponding largely to subgenus Streptocarpus, lack a vegetative SAM and therefore have no erect vegetative stem. Some acaulescent species, termed unifoliate, have a single leafy organ (a phyllomorph) that arises by continued growth of one cotyledon after germination (Figure 1A; Jong, 1970, 1978; Jong and Burtt, 1975; Burtt, 1994). In other species, additional phyllomorphs are produced from existing phyllomorphs without involving a conventional SAM. Such plants are rosette like and are called rosulate (Figure 1C). Acaulescent species are able to abscise the distal part of the phyllomorph under drought conditions and hence colonize drier and more seasonal habitats than caulescent species (Burtt, 1998). Although lacking a conventional vegetative SAM, all acaulescent species form inflorescence meristems that arise from phyllomorph midribs and produce bracts and flowers conventionally (Figures 1A and 1C). Whereas unifoliate species are monocarpic and die after flowering, rosulate plants are perennial.
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, 1942, 1964). In some acaulescent species, application of gibberellic acid (GA) resulted in either the formation of extra phyllomorphs or induction of a vegetative shoot (Rosenblum and Basile, 1984).
Studies in model species have demonstrated the importance of Class I KNOTTED-like homeobox (KNOX) genes in SAM function and leaf development. Several of the effects of altered KNOX activity resemble the morphological differences among Streptocarpus species. For example, Arabidopsis thaliana mutants lacking activity of the KNOX gene SHOOT MERISTEMLESS (STM) do not form a SAM during embryogenesis (Barton and Poethig, 1993), as in acaulescent Streptocarpus species. In weaker stm mutants, leaves are formed from the base of cotyledons or existing leaves, apparently without the involvement of a SAM (Clark et al., 1996), resembling rosulate acaulescent Streptocarpus. Gain-of-function KNOX mutations that cause misexpression in leaves can have the opposite effect of conferring meristematic properties on the leaf. These properties are manifest as ectopic leaf outgrowths, and occasionally, SAMs (reviewed in Tsiantis and Hay, 2003), and therefore mimic the morphologies of acaulescent Streptocarpus. A further suggestion that altered KNOX activity might be involved in the novel morphology of Streptocarpus is that KNOX activity is able to repress GA biosynthesis (Sakamoto et al., 2001; Hay et al., 2002), and unifoliate Streptocarpus can phenocopy caulescent Streptocarpus when they are treated with GA, suggesting that acaulescent morphology might involve reduction of GA levels by KNOX activity (Rosenblum and Basile, 1984).
To further investigate the role of KNOX activity in Streptocarpus evolution, we isolated paralogous STM-like genes, SSTM1 and SSTM2, from a range of Streptocarpus species. We found SSTM1 expression in leaves of rosulate but not unifoliate species, suggesting that changes in SSTM1 expression have been involved in evolution of novel morphologies. We were able to attribute rosulate and unifoliate morphologies to genetic differences at two loci, although neither locus was found to correspond to SSTM1. This suggested that mutations in SSTM1 itself have not been responsible for altered gene expression or morphology.
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RESULTS |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
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, 1998). Phylogenetic comparison of the SSTM1 sequences with those of other KNOX genes placed them together in a well-supported clade with STM but no other Arabidopsis gene (Figure 2B). The SSTM1 genes were therefore likely to be orthologs of Arabidopsis STM.
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High stringency hybridization with the homeobox probe detected two to three strongly hybridizing fragments in each species and 4 to 10 additional fragments that hybridized weakly (Figure 3A). At low stringency, two additional fragments were detected in S. dunnii and S. rexii (Figure 3B). This suggested that the KNOX gene family comprises 6 to 14 members in Streptocarpus. High stringency hybridization with either the 5' region of SSTM1 or its 3' region detected a minimum of two fragments in each species, supporting the existence of two STM-like genes in Streptocarpus (Figures 3C and 3D).
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More than one sequence was amplified from many species, supporting the presence of two STM-like genes. Parsimony analysis of the highly conserved exon sequences did not fully resolve gene relationships (Figure 4A). Intron sequences from the SSTM1 genes of three species—S. saxorum, S. pallidiflorus, and S. glandulosissimus—could not be included in the intron phylogeny because they contained direct imperfect repeats of 100 nucleotides (see Supplemental Figure 1A online). However, analysis of aligned intron sequences from remaining species placed the genes into two clades (Figure 4B). This suggests that STM-like genes duplicated before the subgeneric split between Clades I and II Streptocarpus. One gene clade was identified as SSTM1 (on the basis of exon sequence shared with cDNAs) and the second designated SSTM2.
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KNOX Expression in Streptocarpus
To determine whether changes in KNOX activity may have been involved in the evolution of Streptocarpus, we compared SSTM1 expression patterns by reverse transcription and PCR in different growth forms. In caulescent S. saxorum, expression was detected in apical tissues containing vegetative SAMs or inflorescence meristems and at a low level in the proximal leaf petiole but not in other parts of the leaf (Figure 5A). In unifoliate S. dunnii, no SSTM1 expression was detected in leaves (plants had no inflorescences) or the petiolode (Figures 5B and 5D), although transcripts were detected in inflorescence apices using the same method (data not shown). In the rosulate S. rexii, SSTM1 was expressed in the inflorescence apex but not in the leaf or distal midrib. However, in contrast with unifoliate S. dunnii, SSTM1 expression was also detected in the S. rexii petiolode in the region from which further phyllomorphs were initiating (Figures 5C and 5D).
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). The caulescent S. saxorum produces alternate whorls of three leaves from a flat SAM (Figure 6A). KNOX protein was detected in the SAM, visible as a triangular domain between the bases of existing leaf primordia in a transverse section (Figure 6B). In longitudinal sections, protein accumulation was seen in the SAM, axillary meristems, and provasculature extending into leaves but not at the sites of leaf initiation in the SAM (Figure 6D). Signal was detected in leaves at later developmental stages (e.g., Figure 6C), suggesting that the absence of KNOX protein from the site of leaf initiation is transient. In newly initiated leaves, KNOX protein accumulated in two to three layers of cells abaxial to the prospective palisade mesophyll and persisted in these cells at the growing leaf margins and developing vasculature (Figures 6E to 6G) before becoming restricted to the vasculature (Figures 6H to 6J).
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Two Loci Determine the Differences in Form in Clade II Streptocarpus
To examine the genetic basis for the differences in form in Clade II Streptocarpus, we crossed the rosulate S. rexii with two unifoliate species: S. dunnii or S. wittei. F1 hybrids, which were rosulate in form (Figure 1D), were backcrossed to the unifoliate parent. The forms of the S. wittei backcross progeny (n = 112) were scored in juvenile and adult plants, and the S. dunnii backcross progeny (n = 16) were scored only at maturity (Table 1; see supplemental data online). Plants with one major phyllomorph were classed as unifoliate and those with more than one as rosulate. Previous studies had suggested that the rosulate character was determined by a dominant allele at either of two loci: one promoting the rosulate character early in development, the other acting later (Oehlkers, 1938, 1942, 1964). If this were the case, the F1 plants should have been heterozygous at both loci and therefore rosulate. Approximately half their backcross progeny should have inherited the early acting dominant allele and have developed the rosulate character early. Only 39% of the S. wittei backcross progeny (44/112) were scored as rosulate while juvenile, providing no support for the action of an early-acting dominant allele (P = 0.023 in a 
2 test). If dominant alleles of two unlinked loci were responsible for the rosulate morphology at maturity, 75% of the backcross progeny should have inherited at least one dominant allele sufficient to specify rosulate morphology. At maturity, 76% (98/128) of the S. wittei backcross progeny had rosulate morphology, consistent with the action of dominant alleles at two loci that come into effect gradually during development (Table 1; see supplemental data online). The frequency of rosulate plants in the small S. dunnii backcross population was also consistent with the action of two loci.
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If dominant alleles at two loci, R1 and R2, determine rosulate morphology, the rosulate S. rexii parent will have been homozygous R1/R1 R2/R2 and the S. dunnii or S. wittei parent homozygous for the recessive alleles r1 and r2. The F1 S. rexii x unifoliate hybrids will have been heterozygous at both loci and their backcross progeny composed of four different genotypes (R1/r1 R2/r2, R1/r1 r2/r2, r1/r1 R2/r2, or r1/r1 r2/r2) in equal proportions. Rosulate progeny would carry at least one dominant R1 or R2 allele.
SSTM1 genotypes of the backcross population were determined by amplification of an 400-bp region of SSTM1 followed by digestion with a restriction enzyme that cuts the S. dunnii or S. wittei products once and the S. rexii product twice to yield two smaller fragments (Figure 8). As expected, approximately half (62/128) of the backcross progeny were found to be homozygous for the SSTM1 allele from the unifoliate parent, and the remainder were heterozygous (Table 1; see supplemental data online). If SSTM1 is one of the R loci, unifoliate backcross progeny (r1/r1 and r2/r2) should all be homozygous for the SSTM1 allele from the unifoliate parent, and all plants carrying the S. rexii SSTM1 allele should be rosulate. Neither of these criteria were fulfilled in the backcross populations (Figure 8, Table 1; see supplemental data online), suggesting that SSTM1 is not one of the two loci that specifies the morphological differences between unifoliate and rosulate Streptocarpus.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
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Changes in KNOX Activity Accompanied Evolution of Novel Morphologies
All Old World Gesneriaceae whose early growth has been examined have suppressed plumule development and unequal cotyledon development (anisocotyly). These traits are thought to give the seeds a boost in growth when they germinate, as there is little energy stored (Burtt, 1970, 1994). Taken to its extreme, this pattern of growth results in acaulescence, and the cotyledon gives rise to the first (rosulate species) or only phyllomorph (unifoliate species).
In Arabidopsis, caulescence requires STM to promote SAM activity and repress leaf fate (Barton and Poethig, 1993; Byrne et al., 2000). STM is expressed in cells of the SAM but not in cells that will form leaf primordia (Long et al., 1996)—a pattern of expression that is conserved in diverse seed plants (e.g., Jackson et al., 1994; Sundas-Larsson et al., 1998) and that makes STM expression a marker for SAM cell identity. In Arabidopsis, the domain of STM expression overlaps with those of other Class I KNOX genes that are largely restricted to the SAM (e.g., Lincoln et al., 1994; Chuck et al., 1996).
This pattern of KNOX protein expression was also seen in S. saxorum, suggesting conservation of KNOX function in promoting activity of the SAM in caulescent Streptocarpus. However, KNOX proteins also accumulated in S. saxorum leaf primordia after they had initiated from the SAM. Proteins were present in a layer of cells at the adaxial–abaxial boundary and later restricted to cells of the developing leaf vasculature. A very similar pattern of KNOX expression in leaves has been described for various taxa with compound leaf primordia, which form either compound leaves or derived simple leaves (Bharathan et al., 2002). A causal relationship between KNOX activity and compound leaf development has also been demonstrated in Arabidopsis and tobacco (Nicotiana tabacum), where ectopic KNOX expression in leaves causes compounding (e.g., Chuck et al., 1996; Hay et al., 2003), and in the compound leaves of tomato (Lycopersicon esculentum), where increased KNOX activity increases the degree of compounding (e.g., Hareven et al., 1996). S. saxorum provides an exception to the correlation between KNOX expression and compound leaf morphology because, like all caulescent Streptocarpus, it produces simple leaves from simple primordia. This suggests that downstream targets of KNOX regulation needed for compounding in other taxa were either unresponsive or lost in Streptocarpus. Known targets of KNOX repression include genes needed for synthesis of GA phytohormones (e.g., Sakamoto et al., 2001). GA signaling is needed for compound leaf development in response to ectopic KNOX expression in Arabidopsis and in tomato leaves that normally express KNOX genes (Hay et al., 2002). Uncoupling of GA biosynthesis from KNOX control could explain why S. saxorum leaf development appears insensitive to KNOX expression.
Previous histological studies have suggested that acaulescent Streptocarpus might retain a vegetative SAM, albeit in an unconventional position (Jong and Burtt, 1975). Cells between the embryonic cotyledons of acaulescent species show the layered arrangement of conventional SAMs but do not contribute to growth after germination. Instead, a SAM-like structure subsequently appears in the petiole of the dominant cotyledon and later gives rise to inflorescence meristems as the groove meristem. This lead to the suggestion that the groove meristem represents a vegetative SAM displaced into the cotyledon petiole (termed the petiolode in this case; Jong and Burtt, 1975).
Our expression analyses with S. dunnii, a unifoliate acaulescent species, suggest that this is not the case because we detected no SdSTM1 expression in juvenile plants. Our immunolocalizations corroborated this result in that we did not always detect KNOX protein accumulation in plants lacking conspicuous inflorescences. However, we did detect protein accumulation in inflorescence meristems. Thus, our results suggest that the groove (inflorescence) meristem initiates de novo in S. dunnii and is therefore not equivalent to a conventional SAM. This implies that the vegetative SAM was lost in evolution of the unifoliate growth form. The loss of KNOX expression needed for SAM formation in other angiosperms is consistent with the lack of a vegetative SAM in unifoliate Streptocarpus. SSTM1 expression initiates as the inflorescence meristem initiates, suggesting that a change in the pattern of SSTM1 expression, rather than a complete loss of SSTM1 function, accompanied evolution of the unifoliate growth form.
Although the rosulate S. rexii also appears to lack a vegetative SAM, it expresses SSTM1 and possibly other Class I KNOX genes in the mounds of petiolode cells from which phyllomorphs initiate. These mounds have also been suggested to arise from the groove meristem (Jong, 1978), although we have no direct evidence for this origin, and they may initiate de novo. They therefore resemble conventional SAMs in their structure, expression of SSTM1, and ability to form organs but may be unable to produce organs reiteratively (indeterminacy) and might therefore result from redeployment of only part of the mechanism needed for SAM formation and function. The full mechanism is presumably employed on formation of inflorescence meristems from the groove meristem.
In Streptocarpus, we found that the difference in SSTM1 between a unifoliate and rosulate species correlated with the formation of additional phyllomorphs from SAM-like structures. Crosses between rosulate and unifoliate Streptocarpus indicated that the rosulate character, and hence vegetative SSTM1 expression, was specified by dominant alleles at two loci. Neither locus corresponded to SSTM1. This suggested (1) that vegetative SSTM1 expression was not sufficient to specify the SAM-like structures of rosulate Streptocarpus and (2) that the differences in SSTM1 expression were not the result of differences in SSTM1 alleles themselves but in the genetic prepattern of other factors that regulate SSTM1 expression.
These conclusions are consistent with the findings from Arabidopsis and other model angiosperms that have shown that STM is only one of several genes required for normal SAM formation and function (reviewed in Veit, 2004). Other genes include WUSCHEL (WUS), which is expressed independently of STM and also required for SAM indeterminacy (Mayer et al., 1998). WUS or STM activity alone is insufficient for SAM formation, but WUS and STM together specify at least transient SAMs (Gallois et al., 2002). Expression of cofactors like WUS might therefore be required for the vegetative SAM-like structures of rosulate Streptocarpus. Other genes are known to promote STM and WUS expression, including the CUP-SHAPED COTYLEDON (CUC) genes that are both necessary and sufficient for STM expression and SAM formation in Arabidopsis (Takada et al., 2001). Therefore, differences in regulatory genes like CUC might underlie the evolutionary differences between unifoliate and rosulate Streptocarpus and between caulescent and acaulescent species.
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METHODS |
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TOPABSTRACTINTRODUCTIONRESULTSDISCUSSIONMETHODSREFERENCES |
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and for DNA gel blot hybridizations using the method of Chen and Dellaporta (1994).
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). Nested amplification was performed using primers PHRILL (5'-CCRCACTACCCTCGCCTCTT-3') and Qo (Frohman, 1995), then MEINOX1 (5'-CGCCTGAAGTKGTGGCAAAG-3') and Qi (Frohman, 1995). The same PCR conditions were used as for amplification from genomic DNA, except that annealing was performed at 55°C with primers at a final concentration of 0.2 mM.
For 5' RACE, reverse transcription was primed with ELKup (5'-GCTTGGGGRTCAATGAAACTGT-3') and cDNA products ligated to an adaptor (Siebert et al., 1995). DNA was amplified using primers MEINOX2 (5'-AAGGGCTTTGAACTGRCAYTC-3') and LAPCRT3 (Siebert et al., 1995).
To test for the presence of transcripts in different tissues, total RNA was treated with DNase and used in reverse transcription with Qt primer. Multiplex PCR was then performed with two SSTM1 primers, MegsD (5'-CACGCAGTAGTGTGTGTAATGGAG-3') and ELKup, and two primers for a constitutively expressed Streptocarpus gene, ribosomal up (5'-CCTGCAACTTGGTGGTACGGTA-3') and ribosomal down (5'-CGACACACCCCTGGTACTTT-3') as a control. Both primer pairs span introns. SSTM1 products were detected by DNA gel blot hybridization with a DIG-labeled probe from the conserved region of S. rexii SSTM1 (see below).
For DNA gel blot hybridization, 5 µg of genomic DNA was digested with EcoRI, EcoRV, or HindIII. Fragments were separated, blotted, and hybridized as by Langdale et al. (1991). High stringency hybridization was performed in 3x SSC (1x SSC is 0.15 M NaCl and 0.015 M sodium citrate) at 65°C and low stringency hybridization in 5x SSC at 58°C.
Immunolocalizations were performed essentially according to Donlin et al. (1995) using paraffin embedded tissue. The anti-STM antibody (a gift from Kathy Barton) was used at 1:500 dilution and detected with an alkaline-phosphatase conjugated secondary antibody. Nonspecific binding was blocked with 10% horse serum in PBS containing 0.1% BSA.
Sequence Alignment and Phylogenetic Analysis
SSTM1 and SSTM2 intron sequences were aligned manually using Se-Al v2.0a11 (Rambaut, 1996). ITS sequences were aligned as discussed previously (Möller and Cronk, 2001), except that gaps no longer necessary in the reduced data set were removed. Sequences for the placement of SSTM1 within the KNOX gene family were aligned using ClustalW and adjusted manually using Se-Al v2.0a11. Positions that were not unambiguously alignable were excluded from analyses. The KNOX phylogeny was rooted on Aaknox1 (an algal KNOX gene that shows features of Class I and Class II KNOX genes). To verify that Class I KNOX genes fell in a separate clade from Class II genes, two Class II genes (mkn1 from a moss and Crknox3 from a fern) were also included. Accession numbers of KNOX sequences are given in Table 4 (see supplemental data online), and alignments have been submitted to TreeBASE (www.treebase.org/treebase/).
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) was used to generate Streptocarpus phylogenies. For all analyses, heuristic searches were performed using parsimony. Trees were started using stepwise addition, followed by 5000 random addition sequence replicates and then swapping on best trees. Branch swapping used tree bisection and reconnection with the MULTREES option on. For each addition sequence replicate, two trees of score 
5 were saved. Tree statistics are shown in Table 5.
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Acknowledgments |
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Footnotes |
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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: Jill Harrison (jill.harrison{at}plants.ox.ac.uk).
Online version contains Web-only data.
Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.104.028936.
Received November 1, 2004; accepted November 24, 2004.
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