, Volume 208, Issue 1, pp 129–141 | Cite as

Plasticity in the self-incompatibility system of cultivated Nicotiana alata

  • Jugou Liao
  • Jinran Dai
  • Hongmei Kang
  • Kongfeng Liao
  • Wenguang Ma
  • Jianguang Wang
  • Suiyun Chen


Nicotiana alata has long been a model species for studying gametophytic self-incompatibility (SI) in Solanaceae. Genetically based SI systems are widespread in flowering plants and function to reduce homozygosity and avoid inbreeding depression. However, out-crossing is always unfulfillable for populations with few S-alleles, such as in cultivated clonal populations or populations founded by few individuals. Under such conditions, there is a pressing demand to self-reproduce and pass on genetic information. We carried out a series of pollination and pollen tube observation experiments to explore how homozygous self-incompatible N. alata (S-allele identified and S-RNase active) sets fruits and to explore pseudo-self-fertility in these individuals. We observed several kinds of pollen tube abnormalities, including swelling, furcation, curve and inflexion, tip bursting and irregular callose plug deposition for flowers pollinated at different developmental stages. In addition, SI strength in this line of N. alata plants changed with floral age and flowering stages. That is, flowers became more self-compatible with floral aging, and SI strength in flowers at the end of flowering stages (stage III) was lower and more fruits were set at the top of the pseudo-raceme. Finally, SI strength also varied between individual flowers at the same plant and development stages. However, SI strength varied insignificantly among cultivated N. alata plants homozygous for the same S-allele. These findings indicate that SI in N. alata is plastic, with fruits set by aging flowers, especially flowers at stage III.


Nicotianaalata Self-incompatibility (SI) Pseudo-self-fertility (PSF) Pollination Pollen tubes 



This study was partly supported by grant 31560419 from the National Natural Science Fund in China.

Supplementary material

10681_2015_1606_MOESM1_ESM.tif (128 kb)
Supplementary material 1 (TIFF 128 kb) Generalized features of the S-allele, cited from "Genetic and environmental causes and evolutionary consequences of variations in self-fertility in self incompatible species". Comparison of allelic S-RNase from several Solanaceous species reveals that all S-alleles contain five conserved regions (C1-C5) and two hypervariable regions (HVa and HVb)
10681_2015_1606_MOESM2_ESM.tif (4.2 mb)
Supplementary material 2 (TIFF 4297 kb) N. alata flowers at different developmental stages and the corresponding stigma receptivity. a. Flowers in bud stage and stigma receptivity. b. Flowers at anthesis and stigma receptivity. c. Flowers on the 1st to 2nd day after anthesis and stigma receptivity. d. Flowers on the 3rd–4th days after anthesis and stigma receptivity. e. Flowers 6 days after anthesis and stigma receptivity. f, g. Flowers 9–10 days after anthesis and stigma receptivity
10681_2015_1606_MOESM3_ESM.tif (5.4 mb)
Supplementary material 3 (TIFF 5541 kb) N. alata plants at different developmental stages. a. Stage I, the 12th day from the day when the first flower opened. b. Stage II, the 65th day from the day when the first flower opened. c. Stage III, 103th day from the day when the first flower opened. d, e. Fruit set at stage III


  1. Ai Y, Kron E, T-h Kao (1991) S-alleles are retained and expressed in a self-compatible cultivar of Petunia hybrida. Mol Gen Genet 230:353–358CrossRefPubMedGoogle Scholar
  2. Ascher PD, Peloquin S (1966) Effect of floral aging on the growth of compatible and incompatible pollen tubes in Lilium longiflorum. Am J Bot 53:99–102CrossRefGoogle Scholar
  3. Becerra JX, Lloyd DG (1992) Competition-dependent abscission of self-pollinated flowers of Phormium tenax (Agavaceae): a second action of self-incompatibility at the whole flower level? Evolution 46:458–469CrossRefGoogle Scholar
  4. Broothaerts W, Vanvinckenroye P, Decock B, Van Damme J, Vendrig J (1991) Petunia hybrida S-proteins: ribonuclease activity and the role of their glycan side chains in self-incompatibility. Sex Plant Reprod 4:258–266CrossRefGoogle Scholar
  5. Brown PH, Ho T-HD (1986) Barley aleurone layers secrete a nuclease in response to gibberellic acid purification and partial characterization of the associated ribonuclease, deoxyribonuclease, and 3′-nucleotidase activities. Plant Physiol 82:801–806PubMedCentralCrossRefPubMedGoogle Scholar
  6. Busch JW, Schoen DJ (2008) The evolution of self-incompatibility when mates are limiting. Trends Plant Sci 13:128–136CrossRefPubMedGoogle Scholar
  7. Cruz-Garcia F, Hancock CN, McClure B (2003) S-RNase complexes and pollen rejection. J Exp Bot 54:123–130CrossRefPubMedGoogle Scholar
  8. Dodds PN, Bönig I, Du H, Rödin J, Anderson MA, Newbigin E, Clarke AE (1993) S-RNase gene of Nicotiana alata is expressed in developing pollen. Plant Cell Online 5:1771–1782CrossRefGoogle Scholar
  9. Elgersma A, Stephenson AG, Nijs APM (1989) Effects of genotype and temperature on pollen tube growth in perennial ryegrass (Lolium perenne L.). Sex Plant Reprod 2:225–230CrossRefGoogle Scholar
  10. Fisher RA (1941) Average excess and average effect of a gene substitution. Ann Eugen 11:53–63CrossRefGoogle Scholar
  11. Franklin-Tong NV, Franklin FCH (2003) Gametophytic self-incompatibility inhibits pollen tube growth using different mechanisms. Trends Plant Sci 8:598–605CrossRefPubMedGoogle Scholar
  12. Giblin DE (2005) Variation in floral longevity between populations of Campanula rotundifolia (Campanulaceae) in response to fitness accrual rate manipulation. Am J Bot 92:1714–1722CrossRefPubMedGoogle Scholar
  13. Goldberg EE, Kohn JR, Lande R, Robertson KA, Smith SA, Igić B (2010) Species selection maintains self-incompatibility. Science 330:493–495CrossRefPubMedGoogle Scholar
  14. Goldraij A, Kondo K, Lee CB, Hancock CN, Sivaguru M, Vazquez-Santana S, Kim S, Phillips TE, Cruz-Garcia F, McClure B (2006) Compartmentalization of S-RNase and HT-B degradation in self-incompatible Nicotiana. Nature 439:805–810CrossRefPubMedGoogle Scholar
  15. Good-Avila SV, Stephenson AG (2002) The inheritance of modifiers conferring self-fertility in the partially self-incompatible perennial, Campanula rapunculoides L. (Campanulaceae). Evolution 56:263–272PubMedGoogle Scholar
  16. Good-Avila SV, Mena-Alí JI, Stephenson AG (2008) Genetic and environmental causes and evolutionary consequences of variations in self-Fertility in self incompatible species. Springer, Berlin, pp 33–51Google Scholar
  17. Igic B, Kohn JR (2001) Evolutionary relationships among self-incompatibility RNases. Proc Natl Acad Sci 98:13167–13171PubMedCentralCrossRefPubMedGoogle Scholar
  18. Jahnen W, Batterham MP, Clarke AE, Moritz RL, Simpson RJ (1989) Identification, isolation, and N-terminal sequencing of style glycoproteins associated with self-incompatibility in Nicotiana alata. Plant Cell Online 1:493–499CrossRefGoogle Scholar
  19. Juárez-Díaz JA, McClure B, Vázquez-Santana S, Guevara-García A, León-Mejía P, Márquez-Guzmán J, Cruz-García F (2006) A novel thioredoxin h is secreted in Nicotiana alata and reduces S-RNase in vitro. J Biol Chem 281:3418–3424CrossRefPubMedGoogle Scholar
  20. Laskowska D, Doroszewska T, Depta A, Kursa K, Olszak-Przybys H, Czubacka A (2013) A survey of Nicotiana germplasm for resistance to Tomato Spotted Wilt Virus (TSWV). Euphytica 193:207–219CrossRefGoogle Scholar
  21. Levin DA (1996) The evolutionary significance of pseudo-self-fertility. Am Nat 148:321–332CrossRefGoogle Scholar
  22. Lloyd DG (1992) Self-and cross-fertilization in plants. II. The selection of self-fertilization. Int J Plant Sci 153:370–380CrossRefGoogle Scholar
  23. Lloyd DG, Schoen DJ (1992) Self-and cross-fertilization in plants. I. Functional dimensions. Int J Plant Sci 153:358–369CrossRefGoogle Scholar
  24. Lush WM, Adrienne EC (1997) Observations of pollen tube growth in Nicotiana alata and their implications for the mechanism of self-incompatibility. Sex Plant Reprod 10:27–35CrossRefGoogle Scholar
  25. Mable BK, Dart AVR, Berardo CD, Witham L (2005) Breakdown of self-incompatibility in the perennial Arabidopsis lyrata (Brassicaceae) and its genetic consequences. Evolution 59:1437–1448CrossRefPubMedGoogle Scholar
  26. McClure B (2006) New views of S-RNase-based self-incompatibility. Curr Opin Plant Biol 9:639–646CrossRefPubMedGoogle Scholar
  27. McClure BA, Haring V, Ebert PR, Anderson MA, Simpson RJ, Sakiyama F, Clarke AE (1989) Style self-incompatibility gene products of Nicotlana alata are ribonucleases. Nature 342:955–957CrossRefPubMedGoogle Scholar
  28. McClure B, Mou B, Canevascini S, Bernatzky R (1999) A small asparagine-rich protein required for S-allele-specific pollen rejection in Nicotiana. Proc Natl Acad Sci 96:13548–13553PubMedCentralCrossRefPubMedGoogle Scholar
  29. McClure B, Cruz-García F, Romero C (2011) Compatibility and incompatibility in S-RNase-based systems. Ann Bot 108:647–658PubMedCentralCrossRefPubMedGoogle Scholar
  30. Mena-Ali J, Keser L, Stephenson A (2008) Inbreeding depression in Solanum carolinense (Solanaceae), a species with a plastic self-incompatibility response. BMC Evol Biol 8:1–10CrossRefGoogle Scholar
  31. Meng X, Sun P, T-h Kao (2011) S-RNase-based self-incompatibility in Petunia inflata. Ann Bot 108:637–646PubMedCentralCrossRefPubMedGoogle Scholar
  32. Nasrallah ME, Liu P, Sherman-Broyles S, Boggs NA, Nasrallah JB (2004) Natural variation in expression of self-incompatibility in Arabidopsis thaliana: implications for the Evolution of Selfing. PNAS 101:16070–16074PubMedCentralCrossRefPubMedGoogle Scholar
  33. Nathan Hancock C, Kent L, McClure BA (2005) The stylar 120 kDa glycoprotein is required for S-specific pollen rejection in Nicotiana. Plant J 43:716–723CrossRefPubMedGoogle Scholar
  34. Nielsen LR, Siegismund HR, Philipp M (2003) Partial self-incompatibility in the polyploid endemic species Scalesia affinis (Asteraceae) from the Galápagos: remnants of a self-incompatibility system? Bot J Linn Soc 142:93–101CrossRefGoogle Scholar
  35. Pandey K (1979) Overcoming incompatibility and promoting genetic recombination in flowering plants. N Z J Bot 17:645–663CrossRefGoogle Scholar
  36. Ramakrishnan MN, David MP, Trevor DR, LIan SD, Kate D (2007) Breeding system in Trifolium glanduliferum (Fabaceae). N Z J Agric Res 50:451–456CrossRefGoogle Scholar
  37. Schoen DJ, Morgan MT, Bataillon T (1996) How does self-pollination evolve? Inferences from floral ecology and molecular genetic variation. Philos Trans R Soc Lond Ser B 351:1281–1290CrossRefGoogle Scholar
  38. Singh V, Chauhan SVS (2003) Bud pollination and hybrid seed production in detergent-induced male sterile plants of Brassica juncea. Plant Breed 122:421–425CrossRefGoogle Scholar
  39. Stephenson A, Bertin R (1983) Male competition, female choice, and sexual selection in plants. Pollinat Biol 109:453–458Google Scholar
  40. Stone J (2004) Sheltered load associated with S-alleles in Solanum carolinense. Heredity 92:335–342CrossRefPubMedGoogle Scholar
  41. Stone JL, Sasuclark MA, Blomberg CP (2006) Variation in the self-incompatibility response within and among populations of the tropical shrub Witheringia solanacea (Solanaceae). Am J Bot 93:592–598CrossRefPubMedGoogle Scholar
  42. Stout AB (1931) Pollen-tube behavior in Brassica pekinensis with reference to self-incompatibility in fertilization. Am J Bot 18:686–695CrossRefGoogle Scholar
  43. Travers SE, MENA-ALI J, Stephenson AG (2004) Plasticity in the self-incompatibility system of Solanum carolinense. Plant Species Biol 19:127–135CrossRefGoogle Scholar
  44. Tsukamoto T, Ando T, Kokubun H, Watanabe H, Sato T, Masada M, Marchesi E, Kao TH (2003a) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by a modifier locus that suppresses the expression of an S-RNase gene. Sex Plant Reprod 15:255–263Google Scholar
  45. Tsukamoto T, Ando T, Takahashi K, Omori T, Watanabe H, Kokubun H, Marchesi E, Kao TH (2003b) Breakdown of self-incompatibility in a natural population of Petunia axillaris caused by loss of pollen function. Plant Physiol 131:1903–1912PubMedCentralCrossRefPubMedGoogle Scholar
  46. Vogler DW, Das C, Stephenson AG (1998) Phenotypic plasticity in the expression of self-incompatibility in Campanula rapunculoides. Heredity 81:546–555CrossRefGoogle Scholar
  47. Willi Y (2009) Evolution towards self-compatibility when mates are limited. Eur Soc Evol Biol 22:1967–1973CrossRefGoogle Scholar
  48. Wolters-Arts M, Lush WM, Mariani C (1998) Lipids are required for directional pollen-tube growth. Nature 392:818–821CrossRefPubMedGoogle Scholar
  49. Xu ML, Li YP (2009) Illustrated handbook of tobacco plant resources. Beijing Science Press 779-779Google Scholar
  50. Xu R, Zhu W, Chen J, Wang X, Liu T (2011) Pollen viability and stigma receptivity of Cistanche deserticola. Zhongguo Zhong Yao Za Zhi 36:307–310PubMedGoogle Scholar
  51. Yampolsky C, Yampolsky H (1922) Distribution of sex forms in the phanerogamic flora. Genetica 3:4–62Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2015

Authors and Affiliations

  1. 1.School of Life ScienceYunnan UniversityKunmingChina
  2. 2.Yunnan Academy of ForestryKunmingChina
  3. 3.Tobacco Research InstituteYuxiChina

Personalised recommendations