Skip Navigation


AOBPreview originally published online on September 19, 2007
Annals of Botany 2007 100(6):1373-1378; doi:10.1093/aob/mcm223
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
100/6/1373    most recent
mcm223v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Agricola
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?


© The Author 2007. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Is Eucalyptus Cryptically Self-incompatible?

Tasmien N. Horsley1,2,* and Steven D. Johnson1

1 School of Biological and Conservation Sciences, University of KwaZulu-Natal, Scottsville, South Africa
2 Shaw Research Centre, Sappi Forests, Howick, South Africa

* For correspondence. E-mail: tasmien.horsley{at}sappi.com

Received: 9 May 2007    Returned for revision: 9 July 2007    Accepted: 27 July 2007    Published electronically: 19 September 2007


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

Background and Aims: The probability that seeds will be fertilized from self- versus cross-pollen depends strongly on whether plants have self-incompatibility systems, and how these systems influence the fate of pollen tubes.

Methods: In this study of breeding systems in Eucalyptus urophylla and Eucalyptus grandis, epifluorescence microscopy was used to study pollen tube growth in styles following self- and cross-pollinations.

Key Results: Pollen tubes from self-pollen took significantly longer than those from cross-pollen to grow to the base of the style in both E. urophylla (120 h vs. 96 h) and E. grandis (96 h vs. 72 h). In addition, both species exhibited reduced seed yields following self-pollination compared with cross-pollination.

Conclusions: The present observations suggest that, in addition to a late-acting self-incompatibility barrier, cryptic self-incompatibility could be a mechanism responsible for the preferential out-crossing system in these two eucalypt species.

Key words: Eucalyptus urophylla, Eucalyptus grandis, epifluorescence microscopy, cryptic self-incompatibility


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
To develop sound breeding strategies it is necessary to understand both the reproductive biology and breeding system of a species (Eldridge and Griffin, 1983). The breeding system includes, in its broadest sense, all aspects of sex expression which affect the relative genetic contribution to the next generation of individuals (Wyatt, 1983). Thus an understanding of the breeding system, and the variables that influence it, is essential for a thorough understanding of the ecology, dynamics and long-term viability of populations, and also provides opportunities for commercial exploitation of the species (Ellis and Sedgley, 1992).

Breeding systems of different Eucalyptus species have been investigated using a variety of methods, including isozyme analysis (Moran and Brown, 1980; Yeh et al., 1983; Fripp et al., 1986) and controlled pollinations (Potts and Savva, 1988). However, information on comparative growth rates of self- and cross-pollen in the eucalypt pistil is still lacking. Pollen–pistil interactions have been studied in just eight species to date, viz. Eucalyptus morrisbyi (Potts and Savva, 1988), E. regnans (Sedgley et al., 1989), E. woodwardii (Sedgley, 1989; Sedgley and Smith, 1989), E. spathulata, E. cladocalyx, E. leptophylla (Ellis and Sedgley, 1992), E. globulus (Pound et al., 2002) and E. nitens (Pound et al., 2003).

Eucalyptus is considered to have a breeding system that is preferentially out-crossing, although selfing is not uncommon (Griffin et al., 1987; Eldridge et al., 1994). High out-crossing rates, of between 0·69 and 0·84, have been found in the genus (Moran and Bell, 1983) and are aided by protandry (Pryor, 1976) and reinforced by selection against the products of self-fertilization in later stages of the life cycle (Potts et al., 1987). Most species exhibit a marked reduction in seed yield following self-pollination compared with out-crossing (Potts and Savva, 1988; Ellis and Sedgley, 1992). In fact, there have been reports of more than one self-incompatibility (SI) mechanism operating in a species, which may act at both the pre- and post-zygotic levels (Sedgley and Griffin, 1989). The situation is further complicated by the fact that even in the natural situation, few species are completely selfing or out-crossing, and there are many reports of partial or variable self-incompatibility (Sedgley et al., 1990).

One possible explanation for the variability in out-crossing rates in Eucalyptus is the existence of a system of cryptic self-incompatibility. Cryptic SI usually acts at the stage of pollen tube elongation in the style and leads to faster elongation of cross-pollen tubes relative to self-pollen tubes (Bateman, 1956). As opposed to complete or absolute self-incompatibility, self-pollination without the presence of competing cross pollen in plants with cryptic SI results in successful fertilization and seed set (Bateman, 1956). To date, this type of self-incompatibility has never been associated with Eucalyptus.

The aim of the present study was to examine the breeding systems of Eucalyptus urophylla and E. grandis, by using epifluorescence microscopy to study pollen tube growth in the style following controlled self- and cross-pollinations.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Plant material used in study
The experiments were conducted on mature trees located in clonal (grafted) orchards planted at the Sappi, Shaw Research Centre in KwaZulu-Natal, South Africa. The orchards were situated at 29 °29'S, 30 °11'E at 1100 m a.s.l. Breeding populations for all species were made up of open-pollinated families from selections made in the land-race in South Africa and from provenances in the natural range in Australia. Trees were chosen on the basis of floral abundance and accessibility for hand-pollinations. Two genotypes from each species, viz. M1401 and M1413 from E. urophylla, and P1362 and P1369 from E. grandis, were used as maternal parents in the study. Pollen was also collected from these genotypes for use in self- and intraspecific cross-pollinations.

Pollen collection and processing
For pollen extraction, branches containing ripe flower buds were collected and kept in 100-mL bottles containing water to prevent drying out of the branch. To ensure that there was no contamination from other pollen, all open flowers were removed from the branches before being placed in the laboratory overnight. When the operculum had shed and the filaments unfolded, the anthers were excised and left in a desiccator in the presence of silica gel to dry for approx. 48 h at room temperature. When the relative humidity (RH) in the desiccator had reached 10 %, the dried anthers were sieved through a 30-µm mesh to remove debris. The resulting pollen was placed into polypropylene vials, sealed in glass bottles containing silica gel and stored in a freezer at –10 °C until needed.

In vitro germination
Pollen viability was tested under laboratory conditions before use in controlled pollinations. Pollen was left at room temperature and RH for 8 h to rehydrate. In vitro germination was carried out using 30 % (w/v) sucrose, supplemented with 0·15 mg L–1 boric acid in a liquid medium (Horsley et al., 2007). Pollen from each genotype was placed into glass vials containing the in vitro medium (three replications per genotype) and left to incubate in a germination chamber in a completely randomized design for 48 h at 29 °C. After the required time period had elapsed, 5 µL was transferred from the test-tube to a glass slide. Percentage germination was scored using a light microscope (x100 magnification) to count the number of pollen grains germinated out of a total of 50 grains. Six glass slides per genotype (two slides per test tube) were scored for germination (sub-samples), giving a total of 300 pollen grains counted per treatment. Pollen was deemed to have germinated if the pollen tube length was greater than one-half of the diameter of the pollen grain (Potts and Marsden-Smedley, 1989).

Controlled pollination
Pollinations were carried out using two ramets per genotype of each species. The number of flowers suitable for pollination (in terms of accessibility) determined the number of pistil samples that could be fixed for microscopic analysis. This consequently led to differences in sampling time between the different species. Ripe flower buds were emasculated and isolated at anthesis. Each isolation bag enclosed three umbels, with seven flowers per umbel. Treatments were separately isolated, with only one treatment occurring in an isolation bag. Pollen was applied 7 d later, when the stigmas were receptive, and then re-isolated. For E. urophylla, 1600 flowers were pollinated. Pistil samples were then taken at 24, 30, 48, 96, 120, 144 and 216 h after pollination and immediately fixed in formalin–acetic acid–alcohol (FAA) solution. For E. grandis, 400 flowers were pollinated and pistil samples taken at 24, 48, 72 and 96 h after pollination. Fixed samples of both species were stored at room temperature until needed. Capsules were also left on the tree for estimation of seed yield.

Seed set
All capsules remaining at maturity (12 months after pollination) were harvested and allowed to dry out in the laboratory and release their seed. The number of viable seeds in each capsule was counted. Seeds were considered viable if they were rounded, solid and dark in colour as opposed to flat and of a light-brown colour (Pound et al., 2002). Seed-set data was used to determine the level of self-incompatibility in each species from the following formula:


Formula

where ISI = index of self-incompatibility, Vc = viable seed per flower cross-pollinated and Vs = viable seed per flower self-pollinated (Pound et al., 2002).

Sample preparation for epifluorescence microscopy
For each species, eight pistils from each treatment and time interval were studied. Fixative was removed from the pistil samples by rinsing with tap water. The styles were then excised from the buds and left to soften in 4 N NaOH for either 48 h (E. grandis) or 72 h (E. urophylla). After the required time period had elapsed, NaOH was replaced with tap water and samples left for 60 min to rinse. Samples were then placed in analine blue–0·1 N K3PO4 to stain overnight. The next day, samples were mounted with a drop of glycerol onto glass slides and viewed under UV light. Pollen tubes were studied at five levels in the pistil, viz. stigma surface (0 % style penetration), upper style (25 % style penetration), middle style (50 % style penetration), lower style (75 % style penetration) and base of style (100 % style penetration). The data were summarized as the number of samples per treatment in which pollen tubes had successfully penetrated to the five different regions of the pistil.

Statistical analysis
To test for differences in self- and cross-pollen tube growth in the pistil, analysis of covariance using SPSS Version 13·0 was used to establish the statistical significance of observed differences between treatments within each species, with ‘number of samples with pollen tubes at the base of the style’ as the dependent variable and time as a covariate. A count of pollen tubes at various regions of the style was not possible as pollen tubes were too close to each other to be identified individually. As it was common for more than one capsule to be harvested from within a pollination bag, the mean number of seeds set per flower pollinated was calculated for each bag, and these values were analysed using t-tests. Observed differences between the percentages of capsules set after self- vs. cross-pollinations were compared using G-tests. Pollen viability data were angular transformed prior to analysis of variance and Tukey tests.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
In vitro germination
Significant genotypic differences with respect to in vitro pollen tube growth were displayed by both species (Appendix). Of all the genotypes, E. grandis P1369 had the highest pollen germination (76 ± 2·52 %), while E. grandis P1362 had the lowest (19 ± 2·96 %). For E. urophylla, genotype M1413 pollen had higher in vitro germination (69 ± 3·18) than M1401 pollen (35 ± 0·33).

Seed set following controlled pollinations
Capsule retention following cross-pollination was greater than that following self-pollination in E. urophylla (64 vs. 37 % capsule set), while the opposite occurred in E. grandis (6 vs. 11 % capsule set). However, in both species cross-pollination produced more seeds per flower pollinated compared with self-pollination (Table 1). These differences in average number of seeds per flower were significant in E. urophylla. However, seed yields for E. grandis could not be analysed statistically due to insufficient replication of individual plants. Of the two species, E. urophylla was slightly more self-incompatible (62·5 %) compared with E. grandis (46 %).


View this table:
[in this window]
[in a new window]

  		TABLE 1. Mean number of seeds per flower following self- and cross-pollination in Eucalyptus urophylla and E. grandis, and calculated levels of self-incompatibility

 
In vivo pollen tube growth
Significant differences in the growth rate of self- and cross-pollen tubes were observed in Eucalyptus urophylla (Table 2), with self-pollen tubes taking approx. 120 h to penetrate 100 % of the style, compared with 96 h taken by cross-pollen tubes (Fig. 1A). Self-pollen tubes of E. grandis also showed a slower rate of growth in the style (Table 3), taking 96 h to reach 100 % of the style, compared with the 72 h taken by cross-pollen tubes (Fig. 1B). In addition to the reduced rate of growth, observed pollen tube abnormalities (such as twisting) were increased following selfing in both species (Fig. 2A), although this was not quantified.


Figure 1
View larger version (11K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		FIG. 1. Comparison of in vivo pollen tube growth after controlled self- and cross-pollinations in (A) Eucalyptus urophylla and (B) Eucalyptus grandis. Cross-pollinations were performed within each species (intraspecific).

 


Figure 2
View larger version (104K):
[in this window]
[in a new window]
[Download PowerPoint slide]
  		FIG. 2. Fluorescence micrographs of squashed Eucalyptus styles harvested after different pollination treatments and stained with aniline blue: (A) twisted pollen tubes after self-pollination in E. urophylla; (B) straight pollen tubes after cross-pollination in E. urophylla; (C–E) pollen tube pathway in an E. grandis cross 72 h after pollination where (C) shows pollen grains germinating on the stigma, (D) shows pollen tubes growing in the middle style and (E) shows pollen tubes at the cut end of the style (at the stylar base). Scale bars: (A, B) = 20 µm; (C–E) = 100 µm.

 


View this table:
[in this window]
[in a new window]

  		TABLE 2. Analysis of covariance of in vivo pollen-tube growth after controlled self- and cross-pollinations in Eucalyptus urophylla

 


View this table:
[in this window]
[in a new window]

  		TABLE 3. Analysis of covariance of in vivo pollen-tube growth after controlled self- and cross-pollinations in Eucalyptus grandis

 


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 
For the species in the present study, no evidence of self-incompatibility was found at the stage of pollen adhesion and germination in the stigmatic exudate. The expression of SI occurred as pollen tubes grew down the style and resulted in a reduction in the pollen tube growth rate following self-pollinations, relative to those following cross-pollinations. This self-pollen tube growth retardation is suggested to be a form of cryptic SI and is in agreement with many reports of SI in the Solanaceae (McGuire and Rick, 1954; Hardon, 1967; Ascher, 1976). While this phenomenon has been investigated in several wild plant species (Bateman, 1956; Waser et al., 1987; Aizen et al., 1990), no evidence of selective stylar inhibition of pollen-tube growth has been presented in any of the eucalypt species studied to date. To the authors' knowledge, this is the first study to suggest cryptic SI in Eucalyptus.

Direct measurement of pollen-tube growth in Amsinckia grandiflora (Weller and Ornduff, 1989), Erythronium grandiflorum (Cruzan, 1989) and Delphinium nelsonii (Waser et al., 1987) have also shown differences in pollen tube growth rate between self and cross pollen. As appears to be the case for E. urophylla and E. grandis, these species can be considered cryptically self-incompatible because growth of incompatible pollen tubes was slower than that of compatible ones, rather than being completely inhibited. Recent studies have shown that there may be more plasticity in the growth of self-pollen tubes than has previously been appreciated (Stephenson et al., 2003; Travers et al., 2004). In studies on Solanum carolinense, Stephenson et al. (2003) showed that self-pollen tube growth was arrested when cross-pollen was available, but when cross-pollen was scarce, the growth of self-pollen tubes (and hence the strength of SI) became a quantitative trait that varied among individuals. Stephenson et al. (2003) and Travers et al. (2004) have subsequently suggested that the plasticity in SI systems be viewed as a mechanism that promotes out-crossing by modulating the intensity with which it handicaps the growth of self pollen.

Late-acting self-incompatibility in E. urophylla and E. grandis also seems likely on account of the low number of seeds set following self-pollination relative to the number of self-pollen tubes in the style (pollen tubes were so abundant that they could not be quantified). Pound et al. (2003) came to the same conclusion in their study on E. nitens, where, as in the present study, seed yields were reduced following self-pollinations even though both self- and cross-pollen tubes had grown down the style. Since most self-fertilized E. nitens ovules had begun to degenerate within the first few weeks following pollination instead of being spread over the entire seed development time, Pound et al. (2003) suggested that ovule breakdown was a self-incompatibility response. At present it is difficult to experimentally determine which system is operating within a species. Seavey and Bawa (1986) suggest that uniform ovule abortions may indicate a self-incompatibility response whereas ovule abortions occurring at various stages of embryo development would be indicative of inbreeding depression. However, Waser and Price (1991) question whether inbreeding depression could account for very high levels of ovule abortion.

A potential drawback of the present study is that single-donor pollinations, as opposed to mixed-pollinations, were used to study differences in pollen tube growth rate. The reason for utilizing single-donor pollinations was to avoid the difficulty in distinguishing respective self- and cross-pollen tubes in the style after mixed-pollinations. The sources of pollen included in mixtures could additionally confound breeding system observations, where differences in pollen tube growth rate could be due to differing pollen viability and pollen–pollen interactions (Waser et al., 1987). In a follow-up study, microsatellite markers will be used to distinguish the contribution of self- and cross-pollen to seed set after both single- and mixed-donor pollinations are performed on Eucalyptus grandis. Pollen viability will be used to determine the proportion of each pollen source when making up pollen mixtures.


   APPENDIX
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
ACKNOWLEDGEMENTS
 LITERATURE CITED
 
Appendix 1. In vitro germination of Eucalyptus urophylla and E. grandis pollen used in controlled pollinations


Species Genotype n Mean ± s.e. (%)*
E. grandis P1369 3 76·00 ± 2·52a
E. urophylla M1413 3 68·67 ± 3·18a
E. urophylla M1401 3 34·67 ± 0·33b
E. grandis P1362 3 19·33 ± 2·96c

*Treatments indicated by the same letter are not significantly different; otherwise P < 0·001.


   ACKNOWLEDGEMENTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
LITERATURE CITED
 
Diana Madondo is acknowledged for her help with the controlled pollinations at the Shaw Research Centre. The assistance of the EM Unit staff at the University of KwaZulu-Natal, Pietermaritzburg, and the use of their fluorescence microscope are gratefully acknowledged.


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 APPENDIX
 ACKNOWLEDGEMENTS
 LITERATURE CITED
 

    Aizen MA, Searcy KB, Mulcahy DL. Among- and within-flower comparisons of pollen tube growth following self- and cross-pollinations in Dianthus chinesis (Caryophyllaceae). American Journal of Botany (1990) 77:671–676.[CrossRef][Web of Science]

    Ascher PD. Self-incompatibility systems in floriculture crops. Acta Horticulturae (1976) 63:205–215.

    Bateman AJ. Cryptic self-incompatibility in the wallflower: Cheiranthus cheiri L. Heredity (1956) 10:257–261.

    Cruzan MB. Pollen tube attrition in Erythronium grandiflorum. American Journal of Botany (1989) 76:562–570.[CrossRef][Web of Science]

    Eldridge KG, Griffin AR. Selfing effects in Eucalyptus regnans. Silvae Genetica (1983) 32:216–221.[Web of Science]

    Eldridge KG, Davidson J, Harwood C, Van Wyk G. Eucalypt domestication and breeding (1994) New York, NY: Oxford University Press.

    Ellis ME, Sedgley M. Floral morphology and breeding system of three species of Eucalyptus, section Bisectaria (Myrtaceae). Australian Journal of Botany (1992) 40:249–262.[CrossRef][Web of Science]

    Fripp YJ, Griffin AR, Moran GF. Variation in allele frequencies in the outcross pollen pool of Eucalyptus regnans F. Muell. throughout a flowering season. Heredity (1986) 59:161–171.[Web of Science]

    Griffin AR, Moran GF, Fripp YJ. Preferential outcrossing in Eucalyptus regnans F. Muell. Australian Journal of Botany (1987) 35:465–475.[CrossRef][Web of Science]

    Hardon JJ. Unilateral incompatibility between Solanum pennellii and Lycopersicon esculentum. Genetics (1967) 57:795–808.[Free Full Text]

    Horsley TN, Johnson SD, Stanger TK. Optimising storage and in vitro germination of Eucalyptus pollen. Australian Journal of Botany (2007) 55:83–89.[CrossRef][Web of Science]

    McGuire DC, Rick CM. Self-incompatibility in species of Lycopersicon sect. eriopersicon and hybrids with L. esculentum. Hilgardia (1954) 23:101–124.[Medline]

    Moran GF, Bell JC. Eucalyptus—Tanksley SD, Orton TJ, eds. (1983) Amsterdam: Elsevier. 423–441. Isozymes in plant genetics and breeding, Part B.

    Moran GF, Brown ADH. Temporal heterogeneity of outcrossing rates in alpine ash (Eucalyptus delegatensis R.T. Bak). Theoretical and Applied Genetics (1980) 57:101–105.[Web of Science]

    Potts BM, Marsden-Smedley JB. In vitro germination of Eucalyptus pollen: response to variation in boric acid and sucrose. Australian Journal of Botany (1989) 37:429–441.[CrossRef][Web of Science]

    Potts BM, Savva M. Self-incompatibility in Eucalyptus. In: Pollination ‘88—Knox RB, Singh MB, Troini L, eds. (1988) Melbourne: School of Botany, University of Melbourne. 165–170.

    Potts BM, Potts WC, Cauvin B. Inbreeding and interspecific hybridisation in Eucalyptus gunnii. Silvae Genetica (1987) 30:194–199.

    Pound LM, Wallwork MAB, Potts BM, Sedgley M. Self-incompatibility in Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany (2002) 50:365–372.[CrossRef][Web of Science]

    Pound LM, Wallwork MAB, Potts BM, Sedgley M. Pollen tube growth and early ovule development following self- and cross-pollination in Eucalyptus nitens. Sexual Plant Reproduction (2003) 16:59–69.[CrossRef][Web of Science]

    Pryor LD. The biology of eucalypts (1976) London: Edward Arnold.

    Seavey SR, Bawa KS. Late-acting self-incompatibility in Angiosperms. Botanical Review (1986) 52:195–219.

    Sedgley M. Ovule and seed development in Eucalyptus woodwardii Maiden (Symphyomyrtus). Botanical Gazette (1989) 150:271–280.

    Sedgley M, Griffin AR. Sexual reproduction of tree crops (1989) London: Academic Press.

    Sedgley M, Smith RM. Pistil receptivity and pollen tube growth in relation to the breeding system of Eucalyptus woodwardii (Symphyomyrtus: Myrtaceae). Annals of Botany (1989) 64:21–31.[Abstract/Free Full Text]

    Sedgley M, Hand FC, Smith RM, Griffin AR. Pollen tube growth and early seed development in Eucalyptus regnans F. Muell. (Myrtaceae) in relation to ovule structure and preferential outcrossing. Australian Journal of Botany (1989) 37:397–411.[CrossRef][Web of Science]

    Sedgley M, Bell F, Bell D, Winks C, Pattison S, Hancock T. Self- and cross-compatibility of macadamia cultivars. Journal of Horticultural Science (1990) 65:205–213.[Web of Science]

    Stephenson AG, Travers SE, Mena-Ali JI, Winsor JA. Pollen performance before and during the autotrophic-heterotrophic transition of pollen tube growth. Philosophical Transactions of the Royal Society of London B (2003) 358:1009–1018.[CrossRef]

    Travers SE, Mena-Ali J, Stephenson AG. Plasticity in the self-incompatibility system of Solanum carolinense. Plant Species Biology (2004) 19:127–135.[CrossRef]

    Waser NM, Price MV. Reproductive costs of self-pollination in Ipomopsis aggregata (Polemoniaceae): are ovules usurped? American Journal of Botany (1991) 78:1036–1043.[CrossRef][Web of Science]

    Waser NM, Price MV, Montalvo AM, Gray RN. Female mate choice in a perennial herbaceous wildflower, Delphinium nelsonii. Evolutionary Trends in Plants (1987) 1:29–33.[Web of Science]

    Weller SG, Ornduff R. Incompatibility in Amesinckia grandiflora (Boraginaceae): distribution of callose plugs and pollen tubes following inter- and intramorph crosses. American Journal of Botany (1989) 76:277–282.[CrossRef][Web of Science]

    Wyatt R. Pollinator-plant interactions and the evolution of breeding systems. In: Pollination biology—Real L, ed. (1983) Orlando, FL: Academic Press.

    Yeh FC, Brune A, Cheliak WM, Chapman DC. Mating system of Eucalyptus citriodora in a seed-production area. Canadian Journal of Forest Research (1983) 13:1051–1055.


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?



This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
100/6/1373    most recent
mcm223v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Google Scholar
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Agricola
Right arrow Articles by Horsley, T. N.
Right arrow Articles by Johnson, S. D.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?