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Reproductive Biology |
Department of Biology, 5720 Mayflower Hill Dr., Colby College, Waterville, Maine 04901 USA
Received for publication June 1, 2005. Accepted for publication January 13, 2006.
ABSTRACT
Breakdown of genetically enforced self-incompatibility (SI), an extremely common and important evolutionary transition in plants, has conventionally been conceived as a qualitative rather than a quantitative change. We evaluated qualitative and quantitative variation in SI for four populations of Witheringia solanacea in Costa Rica, examining growth of self-pollen tubes in pollinations of buds and mature flowers. We also measured levels of RNase production in styles to determine whether enzyme production was correlated with differences in self-rejection. The two small populations contained both self-compatible (SC) individuals and obligate outcrossers (female or SI). Plants in the two large populations were uniformly SI as revealed by pollen tube growth, although several of these individuals sporadically set seed autogamously. Stylar RNase activity did not differ significantly between bud and mature flowers, but self-pollen tube growth did differ, suggesting that a gene product in addition to S-RNase is responsible for developmental onset of SI. Population-level differences in RNase activity were consistent with differences in the strength of the rejection response in bud pollinations, suggesting that a threshold level of S-RNase, in combination with other factors, is necessary for SI. Our results support a growing body of evidence that not only qualitative variation in SI, but also quantitative variation may be functionally significant.
Key Words: Costa Rica • mating system • pollen tubes • self-compatibility • self-incompatibility • Solanaceae • S-RNase • Witheringia
Genetically enforced self-incompatibility (SI) mechanisms are widespread in flowering plants. When self pollen is deposited on the stigma of an SI individual, a recognition and rejection response ensures that self-fertilization will not occur. Several distinct genetic and biochemical bases for SI have been identified in unrelated groups (de Nettancourt, 2000
). Gametophytic SI is apparently the ancestral state of the common ancestor of the Rosids and the Asterids and is found in the Solanaceae, the Rosaceae, and the Scrophulariaceae (Igic and Kohn, 2001
). In these families, the female component of the SI response is governed by an S-RNase produced in the style, which enters all pollen tubes and degrades RNA of pollen tubes that fail to be recognized as non-self. The male component of SI is regulated by an F-box protein expressed in the pollen (Sijacic et al., 2004
), but details of the SI response at the biochemical level have yet to be worked out. In addition to the S-RNase and pollen S, numerous other gene products are necessary for the successful functioning of SI (Cruz-Garcia et al., 2003
). Mutations in any of these genes can lead to breakdown of SI, which has occurred frequently in the Solanaceae (Stone, 2002
; Igic et al., 2004
). Polyploidy or duplication of the pollen part of the S-locus acts to eliminate male function of SI by permitting heteroallelic pollen to be recognized as non-self by any S-RNase (Golz et al., 1999
; Tsukamoto et al., 2005
). Loss of female function can result from mutations causing loss of S-RNase activity (Kowyama et al., 1994
; Royo et al., 1994
) or by loss of self-recognition (Golz et al., 1998
). Loss of female function has also been caused by mutation of a non-S-linked gene that produces a stylar protein called HT, whose function is still unknown (McClure et al., 1999
; Kondo et al., 2002b
).
Stebbins (1974
, p. 51) has stated that "the evolutionary pathway from obligate outcrossing based upon self-incompatibility to predominant self-fertilization has probably been followed by more different lines of evolution in flowering plants than has any other." Ecological and geographic correlates of breakdown of SI are well documented. The fate of a mutation that weakens or abolishes the SI response will depend upon the balance between ecological and genetic factors that can either lead to self-fertilization (e.g., reproductive assurance) or eliminate it (e.g., inbreeding depression). Reproductive assurance is especially important in small populations (Baker, 1955
), where low S-allele diversity may limit the number of compatible mates (Byers and Meagher, 1992
; Reinartz and Les, 1994
; Vallejo-Marín and Uyenoyama, 2004
), or where pollinator vectors may be scarce (Barrett et al., 1989
; Fausto et al., 2001
). Biosystematic work has documented numerous examples of centrally located SI species or populations characterized by large population sizes, with derivative self-compatible (SC) species or populations characterized by colonizing lifestyles or peripheral habitats (Stebbins, 1957
; Lloyd, 1980
; Barrett and Shore, 1987
; Wyatt, 1988
; Barrett et al., 1989
; Lipow et al., 1999
). In several species of South American SI Solanaceae, SC populations have been found only at the periphery of the species ranges (Solanum pennellii,Rick and Tanksley, 1981
; Lycopersicon peruvianum, Rick, 1986
; L. hirsutum, Rick et al., 1979
).
In contrast to the solid generalizations garnered from decades of work on ecological and geographic correlates of variation in SI, little is known about the genetic and biochemical basis for intraspecific variation in SI. In particular, little is known about quantitative variation in SI; SI is generally regarded as a qualitative trait although it is composed of quantitative components. One such component of SI is enzymatic activity. Enzymatic activity in the style differs among S-RNases (McClure et al., 1989
; Clark et al., 1990
); enzymatic activity is therefore a quantitative trait even among individuals with fully functioning SI. There are indications that quantitative variation in components of SI can, in some instances, lead to quantitative variation in SI itself. For example, in Solanum chacoense, a particular low-activity S-RNase is fully SI in some genetic backgrounds but shows sporadic SC in others, due to non-S-linked genes causing differences in expression levels and posttranslational modification (Qin et al., 2001
). A growing body of evidence for species with S-RNase systems demonstrates genotype-specific quantitative breakdown of SI under conditions of floral age or low prior fruit set (Good-Avilla and Stephenson, 2002
; Stephenson et al., 2003
), suggesting quantitative control over timing of S-RNase or other enzymatic activity. The relationship between such quantitative SI and complete SC is not clear. Levin (1996)
argued that quantitative SI often serves as an evolutionary transition to complete SC; in contrast, a recent theoretical model suggested that quantitative SI may sometimes be evolutionarily stable (Vallejo-Marín and Uyenoyama, 2004
). In spite of the potential importance of quantitative variation in enzymatic activity in quantitative or leaky SI, only one study to date has documented variation in enzymatic activity in a natural population, and that one focused on the contrast in activity levels of SI and strongly SC individuals (Tsukamoto et al., 1999
).
Species that are entirely SC may have accumulated numerous loss-of-function mutations since the original one that caused SC, so that the causative mutation is unclear. Multiple loss-of-function mutations, for example, have affected the SI response in the cultivated tomato (Kondo et al., 2002a
). In order to document the mechanism underlying the transition from SI to SC, it is useful to work with a species that contains both SI and SC individuals, in which the mutations causing the breakdown are more recent. A polymorphic species can also permit examination of both quantitative variation in SI and complete SC. Recent biosystematic work on the neotropical genus Witheringia has demonstrated polymorphism for SI in W. solanacea, with one of the two populations surveyed containing both SI and SC individuals (Bohs, 2000
). This polymorphism provides a valuable opportunity to examine the evolutionary dynamics of the transition between SI and SC.
Here we investigate the SI response for four Costa Rican populations of W. solanacea. We quantified stylar RNase production and observed pollen tube growth for self pollinations of buds and mature flowers. Specific questions addressed by this research were (1) Is SC in Costa Rican populations of Witheringia solanacea associated with small population size? (2) Is developmental variation in stylar RNase production, from bud to mature flowers, associated with the strength of the SI response? (3) Is intraspecific variation in stylar RNase production associated with strength of the SI response?
MATERIALS AND METHODS
Study species and populations
Witheringia solanacea L'Her is a morphologically variable shrub whose range extends from southern Mexico and the Caribbean to South America (D'Arcy, 1973
). In Costa Rica, it is usually found on rich soils of the Pacific slope from sea level to 1500 m a.s.l. with at least partial sun. It often occurs in banana or bean plantations or along roadsides or trails, where vegetative propagation from machete cutting is common. Its approximately 1-cm-wide pendant flowers are produced year-round in axillary clusters, with typically one to two mature flowers per cluster, at most, per day. Flowers are hermaphroditic, with the exception of those on male-sterile individuals found in one small gynodioecious population. Pollen is the primary reward, and halictid bees are the primary visitors. Flowers last for 2 days, with anthers dehiscing longitudinally several hours after the corolla opens. On the third day after opening, the corolla dehisces, and the pedicel rotates to an upright position if fertilization has occurred. Bird-dispersed berries 1 cm in diameter turn red about 1 month after fertilization.
We sampled four populations, two large continuous ones at Las Cruces and Monteverde and two small isolated ones at Bajos del Toro and Varablanca (Fig. 1). Las Cruces and Varablanca were chosen as a follow up to Bohs' (2000) work, which documented populations as SI or SC/SI but did not report observations of individual plants. The other two populations were chosen after 30 days of reconnaissance, using herbarium records as starting points. The population at Monteverde was the most northwest population that we located, making it the farthest possible distance, within Costa Rica, from Las Cruces. The population at Bajos del Toro was selected for study because of its gender dimorphism, previously unreported in this genus.
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).
Bajos del Toro is a small, isolated roadside population on a steep, south-facing slope in the midst of degraded pastures near the continental divide in the Cordillera Central. Only four plants were found at Bajos del Toro; only one of these four possessed functional stamens. Female plants had greatly reduced, empty anthers. The Varablanca population is a small population in the Rio Sarapiquí valley, east of the continental divide, near the base of the falls of the Rio La Paz Pequeña. It was first located in 1992 by Bohs (2000)
and has been relocated again in 2000 and in 2004. Each time, four to five individuals were found, although the exact locations differed somewhat. In 2004, a 10-day search in surrounding areas failed to locate additional individuals, so we are confident that this population is indeed a small, isolated one. Vouchers from each collection were verified by Lynn Bohs (University of Utah) and deposited at the University of Costa Rica herbarium (voucher numbers Stone 1500–1512). Cuttings were collected in the field and maintained as potted plants in the greenhouse at Colby College (Table 1), where they were used for pollinations and RNase activity assays.
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Pollen tube observations
Pollen tube growth was observed for both bud and mature pollinations for six individuals from each of the Las Cruces and Monteverde populations and from the three available individuals from the Bajos del Toro and Varablanca populations. Styles were stained as described in Martin (1959)
and observed with fluorescence microscopy. Pollen tubes were counted for the stigma, middle of style, and base of the style. Pollen tubes were observed in the ovary when possible. Means for each stage on each individual are based on pollinations of four to six flowers. Individuals were classified as SI or SC based on whether or not pollen tubes reached the base of the style in mature pollinations. To compare pollen tube growth in SI and SC plants, we used Mann-Whitney U tests, due to the unequal sample sizes. For SI individuals in Monteverde and Las Cruces, a t test on means for each individual was used to compare populations for number of pollen tubes at the base of the style in bud pollinations.
RNase activity in styles
RNase activity in styles of mature flowers and buds was estimated for the same individuals used in pollen tube observations. Three separate extractions were done for both mature and bud flowers of most individuals. For each extraction, 10 styles per plant were collected on liquid nitrogen and processed immediately or stored at –80°C. Styles were ground on liquid nitrogen using the extraction buffer of Golz et al. (1998)
; the supernatant was processed immediately or stored at –80°C. Total stylar protein concentrations were determined using a colorometric assay (Bio-Rad, Hercules, California, USA), with BSA as a standard. A spectrophotometric method modified from McClure et al. (1989)
was used to monitor RNase activity. Twenty microliters of buffer-soluble stylar protein was added to 200 µL digestion buffer (0.1 M K3PO4, pH 7, 0.05 M KCl) containing 4 mg/mL torula yeast RNA (Sigma, St. Louis, Missouri, USA). A control was immediately stopped with 55 µL of ice-cold 20% trichloroacetic acid (Tsukamoto et al., 1999
) and placed on ice. The reaction tube was incubated at 37°C for 30 min before stopping, and then incubated together with the control on ice 10 min. Samples were centrifuged at 13000 x g for 15 min at 4°C. Twenty-fold dilutions were made into RNase free water for spectrophotometric readings. The control cuvette was used as a reference for the reaction cuvette, and absorbance at 260 nm was recorded. Dilutions were adjusted as necessary so that the absorbance reading was between 0.1 and 1.0. RNase activity was defined as the increase in absorbance at 260 nm per minute of incubation per milligram of buffer-soluble protein.
The t tests using separate variances were used to compare stylar RNase production for bud vs. mature flowers and SI vs. SC plants. For the two large populations at Monteverde and Las Cruces, which contained only SI individuals, a nested ANOVA was used to compare variation in stylar RNase production. The F statistic for differences between populations used plants within populations as the denominator. Confidence intervals around the standard deviation for pollen tube growth were calculated with sSD = (0.707) SD/
n (Sokal and Rohlf, 1981
). SYSTAT version 5.2.1 (Evanston, Illinois, USA) was used for statistical analysis.
RESULTS
Seed set observations
Two individuals from the Varablanca population displayed repeated autonomous selfing, continually producing spontaneous fruits in the greenhouse. The third individual never produced autogamous fruit. One individual from Bajos del Toro was a strong spontaneous selfer; the other two individuals from Bajos del Toro had greatly reduced anthers, 2.5 mm, in contrast to the norm of 
5 mm for this species. The reduced anthers yielded no pollen in our buzz pollinations; therefore, we could not self-pollinate these individuals. In the two large populations, particular individuals episodically produced large quantities of autogamous fruit. Although most of these individuals produced fruit only several times per year, no other plants in the greenhouse spontaneously produced fruit, suggesting that the fruiting was genuinely autogamous and not due to inadvertent insect pollination. One individual from Monteverde produced seed autonomously almost as consistently as the strong spontaneous selfers from Bajos del Toro and Varablanca.
Pollen tube observations
Pollen tube observations confirmed SC of the most consistently autogamous individuals. For spontaneous selfers from Bajos del Toro and Varablanca, many pollen tubes reached the base of the style in mature self-pollinations. However, the plants from Monteverde and Las Cruces that selfed spontaneously in the greenhouse appeared to be SI according to our assay. Virtually no pollen tubes reached the base of the style in hand self-pollinations of mature flowers (Table 2). Based on pollen tube observations, sporadically autogamous plants were classified as SI, although SI periodically broke down in these individuals.
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For bud pollinations, as for mature pollinations, pollen tube number decreased from stigma to base of style in all cases (Table 3). However, bud pollinations, unlike pollinations of mature flowers, allowed pollen tubes to grow to the base of the style and penetrate ovules for SI as well as SC plants (Fig. 2, Table 3). SI status did not significantly affect the number of pollen tubes reaching midstyle (U = 23, P > 0.10, n1 = 12, n2 = 3) or the base of the style (U = 24, P > 0.10, n1 = 12, n2 = 3) for bud pollinations. The success of bud pollinations at overcoming the SI response differed between populations: significantly more pollen tubes reached the base of the style for bud pollinations of SI individuals from Monteverde than from Las Cruces (Table 3; t = 2.7, df = 10, P < 0.035).
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Loss of SI in small populations
In contrast to the classical view that SI is a solely discrete trait, our results show high levels of quantitative as well as qualitative variation in SI within and among Costa Rican populations of W. solanacea. Complete SC was found only in the two small populations, Bajos del Toro and Varablanca, and co-occurred with obligate outcrossing in both cases. For plants from Bajos del Toro, one individual was strongly SC, while the other two individuals were obligate outcrossers by virtue of being female. For plants from Varablanca, two individuals were strongly SC, while the third had a strong SI response. It is noteworthy that these occurrences of SC were found in small populations at the geographic periphery of the species. Small and geographically peripheral populations are commonly associated with increased self-fertilization, due to poor pollinator service and/or a reduced number of compatible mates (reviewed by Lloyd, 1980
; Wyatt, 1988
; Fausto et al., 2001
). Population size may be a critical component of shift in mating system; geographically peripheral populations of Aquilegia canadensis that were not smaller than centrally located ones did not have increased selfing rates (Herlihy and Eckert, 2005
), and the filter of colonization, rather than current selection pressures, seems to explain increased selfing of Nicotiana glauca introduced to islands in California (Schueller, 2004
). The S-RNase found in SC plants from Vara Blanca is closely related to the "leaky" S-RNase from Monteverde, suggesting that facultatively SC individuals may be more effective colonizers, as suggested by Baker (1955)
.
Self-compatible individuals of W. solanacea had significantly lower stylar RNase activities than did SI individuals. Low stylar RNase production is associated with SC in both Nicotiana (Golz et al., 1998
) and Lycopersicon (Kowyama et al., 1994
; Royo et al., 1994
; Kondo et al., 2002b
). Breakdown of S-RNase function is not necessarily the primary cause of SC in these cases; SC due to a previous mutation could have relaxed selection on loss-of-function mutations for S-RNase. In self-compatible Lycopersicon, absent or decreased S-RNase activity was accompanied by loss of production of the stylar protein HT (Kondo et al., 2002b
), which is necessary for a functional SI response (McClure et al., 1999
). Causes for reduced S-RNase activity in Lycopersicon species were various, including downregulated transcription and posttranslational defects, but the mechanism for reduced HT production was uniformly transcriptional depression. Parsimony suggests, therefore, that the mutation suppressing HT production preceded mutations leading to loss of RNase activity in Lycopersicon. In contrast to most of the SC Lycopersicon species, SC individuals of W. solanacea continue to produce mRNA for S-RNase; RT-PCR has been successful in amplifying S-RNase genes for SC as well as SI individuals (Stone and Pierce, 2005
).
Variation in quantitative components of SI
SI individuals within populations of W. solanacea differed in stylar RNase activity, which is consistent with findings from other species in which different S-RNases differ in activity (e.g., Nicotiana alata, McClure et al., 1989
; Petunia hybrida, Clark et al., 1990
). We also found variation among populations in mean stylar RNase activity. Interpopulation variation in RNase activity appears to be independent of the particular S-alleles assayed because there is considerable overlap in the S-RNases found in these two populations (Stone and Pierce, 2005
). Pollen tube growth also differed between the two large populations with Monteverde plants having lower stylar RNase activity and more pollen tubes reaching the base of the style in bud self-pollinations than plants from Las Cruces. Lower stylar RNase activity at Monteverde, in combination with some other biochemical factor, may contribute to increased pollen tube growth in bud self-pollinations.
Sporadic breakdown of SI was found in the two large populations. For both Las Cruces and Monteverde, several individuals of the 20 plants sampled repeatedly produced fruit in an insect-free greenhouse and yet rejected manually applied self-pollen. It is possible that SI breaks down in these individuals with floral age or low prior fruit set as found in Solanum carolinense (Stephenson et al., 2003
), Campanula rapunculoides (Vogler et al., 1998
) and Leptosiphon jepsonii, which has a sporophytic SI system (Goodwillie et al., 2004
). Delayed floral abscission is associated with breakdown of SI in the individual from Monteverde with the most consistent autogamous fruit production. Its wilted flowers are retained an extra day, in contrast with immediate abscission for non-autogamous SI plants (J. Stone and M. Sasuclark, unpublished data).
Development of stylar RNase and the SI response
S-RNase production is typically lower pre-anthesis than in mature flowers and has been inferred to be a major cause of reduced SI in bud (e.g., Clark et al., 1990
; Kheyr-Pour et al., 1990
). In Witheringia solanacea, however, buds 2 days prior to anthesis produced stylar RNase at levels equivalent to that of mature flowers, yet bud pollinations still had reduced SI. Our assay did not test specifically for S-RNase production; it is possible that the production of non-S RNases made it difficult to distinguish increases in S-RNase at the time of anthesis. This possibility seems unlikely, however, because S-RNase is produced in extremely high concentrations, typically 10–50 mg/mL (Jahnen et al., 1989
) or 40–86% of total stylar RNase in mature flowers (McClure et al., 1989
). In addition, isoelectric gels show that S-RNase proteins of W. solanacea increase dramatically between small and large buds rather than between large buds and open flowers (J. Stone and J. Guay, unpublished data). Another possibility is that reduced SI in the bud is due not to low S-RNase activity, but to lower expression of other genes such as HT necessary for the SI response. In SI Nicotiana alata, self-pollination is successful when the buds are 2.5 cm long, when S-RNase production is 60% of maximum but HT is only 5% of maximum. One day later, when HT production has increased eight-fold, bud self-fertilization is no longer successful (McClure et al., 1999
).
Is there an evolutionary link between quantitative variation in SI and complete SC?
It is unclear whether selection on quantitative variation in SI could provide a pathway to complete SC, or whether distinctly different types of mutations are responsible. Certainly, single mutations at the S-locus can cause an instantaneous loss of SI (Royo et al., 1994
; Golz et al., 2000
), but it remains possible that SC can sometimes arise gradually from quantitative SI. Genetic work reveals that both quantitative variation in SI (Levin, 1996
; Good-Avilla and Stephenson, 2002
) and complete SC ( Ai et al., 1991
; Tsukamoto et al., 2003
) are often governed by modifier loci, rather than by mutations at the S-locus itself. Commonalities between quantitative SI and complete SC have been found at the level of transcription of S-RNases, posttranslational modification of S-RNases, and regulation of the unlinked modifier gene, HT. Transcriptional downregulation of S-RNase has been associated with full SC in Nicotiana (Golz et al., 1988), Lycopersicon (Kondo et al., 2002b
), and for a particular S-RNase allele in Petunia axillaris (Tsukamoto et al., 2003
). Low levels of S-RNase are also associated with quantitative variation in SI, both in transformation experiments (e.g., Matton et al., 1997
), and in natural populations. In Solanum chacoense, the S12-RNase varies greatly in expression level, depending on the genetic background, and is associated with SC in those backgrounds where its expression is lowest (Qin et al., 2001
). Posttranslational modification of S-RNase has also been implicated for both SC and quantitative SI. S-RNases have varying numbers of potential N-glycosylation sites (Golz et al., 1998
). In SC Nicotiana sylvestris, a novel glycosylation site in one of the hypervariable regions is hypothesized to affect self-pollen recognition for an S-RNase with full enzymatic activity (Golz et al., 1998
). Quantitative SC is associated with different degrees of glycosylation of a particular S-RNase in Solanum chacoense in different genetic backgrounds (Qin et al., 2001
). Finally, lack of production of the stylar protein HT has been implicated in full SC in Lycopersicon species (Kondo et al., 1999b), and in quantitative SI in RNAi lines of S. chacoense (O'Brien et al., 2002
). Interestingly, low expression of HT is associated with increased longevity of flowers, as well as with SC, suggesting a possible mechanism for floral age-dependent breakdown of SI.
Levin (1996)
has proposed that quantitative variation in SI (pseudo-self-fertility) could often provide a transitional pathway between SI and complete SC. A recent analytical model (Vallejo-Marín and Uyenoyama, 2004
) demonstrated that the conditions for the transition from SI to SC are less restrictive when governed by a modifier locus, rather than at the S-locus itself, and also found regions of a parameter space in which leaky SI would be evolutionarily stable. Our work supports the idea that quantitative variation in SI and complete SC may sometimes be related. The partial S-RNase sequence for the highly selfing Varablanca plants is almost identical to the single sequence obtained for the individual from Monteverde that, although SI as revealed by hand self-pollinations, had the most frequent autogamous selfing (SRNases WsolS23 and WsolS12; Stone and Pierce, 2005
), suggesting that a change at the S-locus is associated with both leaky SI and complete SC in these plants.
In conclusion, this work reinforces some well-established principles and raises new questions. As expected, we found that SC was most pronounced in small and peripheral locations. Perhaps a surprising result, given classical predictions, was that both small populations were polymorphic, containing both SC and obligately outcrossing individuals. A novel finding was the difference among populations in both stylar RNase activity and onset of SI as revealed by bud self-pollinations. Perhaps, as other workers have suggested, there is a threshold level of S-RNase, below which the effect of levels of modifiers is most pronounced (Clark, 1990; Qin, 2001). Future work will include further investigation of the implications of quantitative variation in components of SI.
FOOTNOTES
1 The authors thank L. Bohs, E. Bello, and O. Vargas for help in locating populations, the Organization for Tropical Studies for logistical support, C. Bevier, S. Dunham, P. Greenwood, J. Guay, J. Mena Ali, and E. Newbigin for technical support, and three anonymous reviewers and the Associate Editor for helpful comments. Financial support was provided by NSF award INT-0305459 and the Clare Boothe Luce Program of the Henry Luce Foundation. 
2 Author for correspondence (jstone{at}colby.edu
)
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