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Specific Polygalacturonase in Distylous Turnera Subulata (Turneraceae)1

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Specific Polygalacturonase in Distylous Turnera Subulata (Turneraceae)1 American Journal of Botany 90(5): 675±682. 2003. CHARACTERIZATION AND LOCALIZATION OF SHORT- SPECIFIC POLYGALACTURONASE IN DISTYLOUS TURNERA SUBULATA (TURNERACEAE)1 A. ATHANASIOU,2 D. KHOSRAVI,F.TAMARI, AND J. S. SHORE3 Department of Biology, York University, 4700 Keele Street, Toronto, Ontario M3J 1P3 Canada We describe for distylous Turnera subulata a polygalacturonase speci®c to short-styled plants that is localized to the style transmitting tissue (the tissue through which pollen tubes grow). The polygalacturonase gene is linked to and may be upregulated by the S allele of the distyly locus. Because of its tissue-speci®c location, the polygalacturonase may be involved in the self-incompatibility response, acting in a complementary or antagonistic manner, or possibly in signalling downstream events. A pollen-speci®c polygalacturonase was also identi®ed and may be a member of a small multigene family of pollen polygalacturonases. The role, if any, played by the pollen polygalacturonase in distyly, is presently unknown. Key words: distyly; heterostyly; immunocytochemistry; polygalacturonase; transmitting tissue; Turnera; Turneraceae. Distyly, a genetic polymorphism that occurs in a wide range povickasii Arbo. In the present study, we extend the work of of ¯owering plant families, has evolved independently at least Athanasiou and Shore (1997) by sequencing, identifying, and 28 times (Arroyo and Barrett, 2000). Distylous populations localizing the proteins in T. subulata. The style-speci®c pro- possess two mating types (long- vs. short-styled morphs) that tein is a polygalacturonase (PG) localized to the transmitting have a reciprocal positioning of male and female reproductive tissue of the short-styled morph of T. subulata. Linkage anal- organs (reciprocal herkogamy), the anthers and stigmas. Both ysis reveals that the style PG gene is linked to and its expres- morphs commonly possess a self- and intra-morph incompat- sion may be upregulated by the S allele of the distyly locus. ibility system that enforces inter-morph mating and prevents The pollen-speci®c protein is also a polygalacturonase. self-fertilization. Despite a long history of use as a model sys- tem in genetics and evolutionary biology (Ornduff, 1992) be- MATERIALS AND METHODS ginning with Darwin (1877), nothing is known of the molec- ular genetic basis of the polymorphism including dimorphisms Protein puri®cation and sequencingÐExtracts of styles from short-styled in reproductive organ lengths, self-incompatibility (SI), or an- plants of T. subulata were run on isoelectric focusing (IEF) gels (Athanasiou cillary characters. and Shore, 1997) and stained with coomassie brilliant blue. The most heavily Genetic studies of distylous species indicate that all dimor- stained protein band with an isoelectric point (pI) of 6.5 was excised from phic characters, including the SI system, commonly appear to the gel and digested with Lys-C. The resulting peptides were fractionated by be determined by a single diallelic locus, where short-styled high-performance liquid chromatography. Individual fractions were subjected plants are usually heterozygous, Ss, and long-styled plants are to Edman degradation and four amino acid sequences were obtained (per- homozygous recessive, ss (Lewis and Jones, 1992). The dom- formed by the Protein Chemistry Core Facility of the Baylor College of Med- inance relationship is reversed in two families (Baker, 1966; icine). Using extracts of anthers, an identical protocol was followed for the Ornduff, 1979). Studies of Primula spp. (Primulaceae) indicate pollen protein (Athanasiou and Shore, 1997). that the distyly locus is actually composed of at least three tightly linked loci that are held in extreme linkage disequilib- DNA sequencingÐDegenerate primers were designed based on partial pep- rium and comprise a supergene (Ernst, 1955; Dowrick, 1956; tide sequences from the style protein. These primers were used to amplify a Lewis and Jones, 1992; Richards, 1997). In fact, distyly is one genomic DNA sequence using the polymerase chain reaction (PCR). The am- of the best examples of a supergene, yet the molecular genetic pli®ed fragment was sequenced. We designed new primers based upon this initial DNA sequence and used 39 RACE (rapid ampli®cation of cDNA 39 basis of the system is unknown, although candidate proteins/ end) to obtain much of the coding sequence (starting with amino acid residue molecules have been proposed (Golynskaya et al., 1976; Shi- 107). Genomic DNA was extracted according to Doyle and Doyle (1987). vanna et al., 1981; Wong et al., 1994; Athanasiou and Shore, Total RNA was extracted from styles (Jones et al., 1985). We used walking 1997). PCR (Katz et al., 2000) to obtain the remainder of 59 end of the sequence Athanasiou and Shore (1997) discovered proteins speci®c from genomic DNA, because 59 RACE failed to yield any new sequence data. to the styles and pollen of the short-styled morph of Turnera Sequencing of both strands was performed on the PCR-ampli®ed DNA using subulata Smith, T. scabra Millsp., and a few plants of T. kra- cycle-sequencing on an ABI373A sequencer (Applied Biosystems, Foster City, California, USA) at the York University Molecular Biology Core Facil- 1 Manuscript received 5 September 2002; revision accepted 5 December ity. 2002. For the pollen protein, we ampli®ed a fragment from genomic DNA using The authors thank AndreÂBeÂdard, Barrie Coukell, Daphne Goring, and Mo- degenerate primers designed from partial peptide sequences. This DNA frag- han Subramanian for helpful advice, Maria Mercedes Arbo for seeds, and ment was used to screen a pollen cDNA library (Athanasiou, 2001). A single Wendy Lezama and Lee Wong for technical assistance. This research was supported by a National Sciences and Engineering Research Council of Can- clone was isolated and both strands of the cDNA were sequenced. The se- ada grant to J.S.S. quence data have been submitted to GenBank and accession numbers may be 2 Current address: Center for the Biology of Natural Systems, Queens Col- found in the Appendix (http://ajbsupp.botany.org/v90). lege of the City University of New York, Flushing, New York 11367 USA. The PCR ampli®cations were generally performed using the following con- 3 Author for correspondence. ditions with minor modi®cations depending upon the primers used: to 1 mL 675 676 AMERICAN JOURNAL OF BOTANY [Vol. 90 (approximately 50 ng) of genomic DNA was added 40.75 mL nuclease-free in 5-bromo-4-chloro-3-indolyl phosphate/nitro blue tetrazolium (NBP-BCIP) water, 1 mL dNTP mix (10 mmol/L each dATP, dCTP, dGTP, dTTP), 1 mL at 378C in the dark. All immunostaining procedures, with the exception of 59 primer (5 pmol/mL), 1 mL39 primer (5 pmol/mL), 5 mL103 buffer (100 the ®nal colorimetric reaction, were carried out with gentle agitation. mmol/L Tris-HCl pH 8.8, 500 mmol/L KCl, 15 mmol/L MgCl2, 1% Triton X-100), and 1.25 units of AmpliTaq DNA polymerase (Perkin Elmer/Applied ImmunocytochemistryÐStyles were vacuum-in®ltrated for 45 min and Biosystems, Foster City, California, USA). The samples were processed in a ®xed for an additional4hin(3:1)ethanol : glacial acetic acid. Styles were PE-9600 thermal cycler (Perkin Elmer, Boston, Massachusetts, USA) for 35 dehydrated through a graded series of ethanol : tertiary butyl alcohol (TBA) cycles at 948C for 1 min, 558C for 1 min, 728C for 2 min, with a ®nal and were ®nally equilibrated to 100% TBA and in®ltrated with Tissueprep extension at 728C for 5 min. The PCR products were run on ethidium bro- wax (Fisher, Nepean, Ontario, Canada) at 628C. Wax-embedded styles were mide-stained agarose gels (0.8% in TBE buffer) to verify the speci®city of cross-sectioned to 7- m thickness. Sections were stored at 4 C for several the PCR reaction and for further gel puri®cation and sequencing. Detailed m 8 weeks without any activity loss. Sections were expanded by ¯oating at 37 C information on PCR, 39 RACE, cloning, library construction, screening, and 8 in double-distilled water (ddH O) and placed on Biobond-coated (Cedarlane, sequencing protocols are found in Athanasiou (2001). 2 Hornby, Ontario, Canada) glass slides. Slides were then placed on a warming tray at 358C (overnight) to adhere the sections to the slides. Slides were passed Phylogenetic analysisÐAmino acid sequences of both the style and pollen through two 15-min changes of histoclear (Sigma, Oakville, Ontario, Canada), proteins were deduced from the cDNA sequences. The amino acid sequences followed by washes in a graded series of ethanol and ddH O ending with we obtained were compared to plant PG sequences recently used in the phy- 2 ddH O and a ®nal wash in buffer (Tris-HCl-NaCl, 100 mmol/L Tris, 120 logenetic analyses (Had®eld et al., 1998; Hong and Tucker, 2000; Torki et al., 2 2000; MarkovicÏ and JanecÏek, 2001; Appendix at http://ajbsupp.botany.org/ mmol/L NaCl, 30 min). Sections were blocked for 30 min by incubation in v90). Amino acid sequences were aligned using Clustal X (Thompson et al., 200 mL of blocking solution (normal goat serum diluted 1/20 in wash buffer). 1997). The N-terminal region (corresponding to the ®rst 85 amino acids of Blocking solution was shaken gently from the slides, which were then incu- the style PG, Fig. 1A) and the last 15 amino acids of the C-terminal region bated with primary antibody diluted 1/100 in wash buffer. Sections were were removed from all sequences because of considerable gap formation. The washed for 3 3 10 min and then incubated with secondary antibody (CY3- truncated sequences were then realigned. Gaps in the sequences were coded conjugated af®nipure goat anti-rabbit IgG, H1L; Jackson ImmunoResearch, as unknowns. The gene tree was constructed using ordinary protein parsimony West Grove, Pennsylvania, USA), for immunodetection.
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