Gynodioecy in knautia arvensis (caprifoliaceae)

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

The gynodioecy of the herbaceous polycarpic Knautia arvensis was studied in the Moscow Region. Eight populations were examined from 2020 to 2024. The plants form two types of flowers, bisexual and pistillate, on three types of individuals: hermaphrodite (only bisexual flowers), female (only pistillate flowers), and gynomonoecious (bisexual and pistillate flowers). The bisexual flowers are complete, tetracyclic, with tetramerous perianth and androecium, and dimerous gynoecium. The marginal flowers of the floral units are irregular (transversely zygomorphic), the median ones are nearly regular (actinomorphic). In the pistillate flowers, rudiments of the androecium are preserved, represented by staminodes that do not produce pollen. Three criteria were revealed to distinguish the flowers of different sexual types: size differences (bisexual flowers are larger than pistillate ones); the ratio of the length of corolla tube to stamen filaments, and the degree of the androecium preservation after the flower fading. In the sex ratio of the eight populations, the hermaphrodite plants prevailed, from 61.5 to 68.8%. The gynomonoecious variant was the rarest, from 2.0 to 6.3%. No changes in the sex ratio in the populations were found over the five years of observation. The size dimorphism of bisexual and pistillate flowers and the presence of gynomonoecious individuals in gynodioecious species are discussed.

Full Text

Restricted Access

About the authors

G. K. Botov

Moscow Pedagogical State University

Author for correspondence.
Email: grishenka.botov@mail.ru
Russian Federation, Moscow

V. N. Godin

Central Siberian Botanical Garden SB RAS

Email: vn.godin@mpgu.su
Russian Federation, Novosibirsk

References

  1. Ashman T.-L., Stanton M.L. 1991. Seasonal variation in pollination dynamics of sexually dimorphic Sidalcea oregana ssp. spicata (Malvaceae). — Ecology. 72(3): 993–1003. https://doi.org/10.2307/1940599
  2. Bailey M.F., Delph L.F. 2007. Sex-ratio evolution in nuclear-cytoplasmic gynodioecy when restoration is a threshold trait. — Genetics. 176(4): 2465–2476. https://doi.org/10.1534/genetics.107.076554
  3. Baker H.G. 1948. Corolla-size in gynodioecious and gynomonoecious species of flowering plants. — Proc. Leeds Philos. Literary Soc. 5(1): 136–139.
  4. Barrett S.C.H., Hough J. 2013. Sexual dimorphism in flowering plants. — J. Exp. Bot. 64(1): 67–82. https://doi.org/10.1093/jxb/ers308
  5. Benevides C.R., Haddad I.V.N., Barreira N.P., de Rodarte A.A.T., Galetto L., de Santiago-Fernandes L.D.R., de Lima H.A. 2013. Maytenus obtusifolia Mart. (Celastraceae): a tropical woody species in a transitional evolutionary stage of the gynodioecy-dioecy pathway. — Plant Syst. Evol. 299(9): 1693–1707. https://doi.org/10.1007/s00606-013-0826-6
  6. Bobrov E.G. 1978. Fam. 130. Dipsacaceae Lindl. — In: Flora of the European part of the USSR. Vol. 3. Leningrad. P. 37–46 (In Russ.).
  7. Casimiro-Soriguer I., Buide M.L., Narbona E. 2013. The roles of female and hermaphroditic flowers in the gynodioecious — gynomonoecious Silene littorea: insights into the phenology of sex expression. — Plant Biol. J. 15(6): 941–947. https://doi.org/10.1111/j.1438-8677.2012.00697.x
  8. Cervantes C., Alvarez A., Cuevas E. 2018. Small but attractive: female-biased nectar production and floral visitors in a dimorphic shrub. — Plant Biol. 20(1): 160–164. https://doi.org/10.1111/plb.12653
  9. Charlesworth D., Laporte V. 1998. The male-sterility polymorphism of Silene vulgaris: analysis of genetic data from two populations and comparison with Thymus vulgaris. — Genetics. 150(3): 1267–1282. https://doi.org/10.1093/genetics/150.3.1267
  10. Connor H.E. 1965. Breeding systems in New Zealand grasses. VI. Control of Gynodioecism in Cortaderia richardii (Endl.) Zotov. — N. Z.J. Bot. 3(4): 233–242. https://doi.org/10.1080/0028825X.1965.10429017
  11. Darwin C. 1877. The different forms of flowers on plants of the same species. London. 352 p.
  12. Delph L.F., Galloway L.F., Stanton M.L. 1996. Sexual dimorphism in flower size. — Amer. Nat. 148(2): 299–320. https://doi.org/10.1086/285926
  13. Demyanova E.I. 1985. Distribution of gynodioecy in flowering plants. — Bot. Zhurn. 70(10): 1289–1301 (In Russ.).
  14. Dommée B., Assouad M.W., Valdeyron G. 1978. Natural selection and gynodioecy in Thymus vulgaris L. — Bot. J. Linn. Soc. 77(1): 17–28. https://doi.org/10.1111/j.1095-8339.1978.tb01369.x
  15. Dudle D.A., Mutikainen P., Delph L.F. 2001. Genetics of sex determination in the gynodioecious species Lobelia siphilitica: evidence from two populations. — Heredity. 86(3): 265–276. https://doi.org/10.1046/j.1365-2540.2001.00833.x
  16. Dufay M., Billard E. 2012. How much better are females? The occurrence of female advantage, its proximal causes and its variation within and among gynodioecious species. — Ann. Bot. 109(3): 505–519. https://doi.org/10.1093/aob/mcr062
  17. Etten Van M.L., Chang S.M. 2014. Frequency-dependent pollinator discrimination acts against female plants in the gynodioecious Geranium maculatum. — Ann. Bot. 114(8): 1769–1778. https://doi.org/10.1093/aob/mcu204
  18. Fedorov Al.A., Artyushenko Z.T. 1975. Organographia illustrata plantarum vascularum. Flos. Leningrad. 351 p. (In Russ.).
  19. Franzén M., Larsson M. 2009. Seed set differs in relation to pollen and nectar foraging flower visitors in an insect-pollinated herb. — Nord. J. Bot. 27(4): 274–283. https://doi.org/10.1111/j.1756-1051.2009.00348.x
  20. Glazunova K.P., Dlusskiy G.M. 2007. Interrelation between flower structure and pollen vector composition in some Dipsacaceae and Asteraceae with externally similar anthodia. — Zhurn. Obsh. Biol. 68(5): 361–378 (In Russ.).
  21. Godin V.N. 2019. Distribution of gynodioecy in APG IV system. — Bot. Zhurn. 104(5): 669–683 (In Russ.). https://doi.org/10.1134/S0006813619050053
  22. Godin V.N. 2020. Distribution of gynodioecy in flowering plants. — Bot. Zhurn. 105(3): 236–252 (In Russ.). https://doi.org/10.31857/S0006813620030023
  23. Godin V.N., Akhmetgarieva L.R. Gynodioecy of Ajuga reptans (Lamiaceae) in Moscow region. — Bot. Zhurn. 104(8): 1211–1227 (In Russ.). https://doi.org/10.1134/S0006813619080027
  24. Godin V.N., Astashenkov A.Y., Cheryomushkina V.A. 2023. Gynodioecy in Nepeta gontscharovii (Lamiaceae). — Bot. Zhurn. 108(2): 155–162 (In Russ.). https://doi.org/10.31857/S0006813623020047
  25. Godin V.N., Astashenkov A.Y., Cheryomushkina V.A., Bobokalonov K.A. 2024. Gynodioecy of Origanum vulgare ssp. gracile (Lamiaceae) in Tajikistan. — Nord. J. Bot. 2024(1): e04148. https://doi.org/10.1111/njb.04148
  26. Godin V.N. 2023. Sexual polymorphism of Ranunculus acris (Ranunculaceae) in the Moscow region. — Bot. Zhurn. 108(1): 13–22 (In Russ.). https://doi.org/10.31857/S0006813622120031
  27. Gordeeva N.I., Komarevtseva E.K. 2020. Variability of the gender spectrum in Origanum vulgare L. (Lamiaceae, Magnoliopsida). — Biol. Bull. Russ. Acad. Sci. 47: 1277–1280. https://doi.org/10.1134/S1062359020100076
  28. Haughn G.W., Somerville C.R. 1988. Genetic control of morphogenesis in Arabidopsis. Dev. Genet. 9(2): 73–89. https://doi.org/10.1002/dvg.1020090202
  29. Jeon Y.-Ch., Moon H.-K., Kong M.-J., Hong S.-P. 2024. Floral dimorphism of Elsholtzia angustifolia (Loes.) Kitag. (Lamiaceae). — Flora. 319: 152583. https://doi.org/10.1016/j.flora.2024.152583
  30. Kamath A., Levin R.A., Miller J.S. 2017. Floral size and shape evolution following the transition to gender dimorphism. — Am.J. Bot. 104(3): 451–460. https://doi.org/10.3732/ajb.1600442
  31. Kamelina O.P., Plisko M.A. 2000. Fam. Dipsacaceae. — In: Comparative anatomy of seeds. Vol. 6. Saint-Petersburg. P. 400–407.
  32. Knuth P. 1898. Handbuch der Blütenbiologie. Bd. II. T. I. Leipzig. 697 S.
  33. Koelewijn H.P., Van Damme J.M.M. 1996. Gender variation, partial male sterility and labile sex expression in gynodioecious Plantago coronopus. — New Phytol. 132(1): 67–76. https://doi.org/10.1111/j.1469-8137.1996.tb04510.x
  34. Larsson M. 2005. Higher pollinator effectiveness by specialist than generalist flower-visitors of unspecialized Knautia arvensis (Dipsacaceae). — Oecologia. 146(3): 394–403. https://doi.org/10.1007/s00442-005–0217-y
  35. Landergott U., Schneller J.J., Holdregger R., Thompson J.D. 2009. Sex ratio variation and spatial distribution of nuclear and cytoplasmic sex determining genes in gynodioecious Thymus praecox across altitudinal gradients. — Evol. Ecol. Res. 11(1): 23–42.
  36. Lecoq H. 1857. Étude sur la géographie botanique de l’Europe et, en particulier, sur la végétation du plateau central de la France. T. 6. Paris. 480 p.
  37. Lewis D., Crowe L.K. 1956. The genetics and evolution of gynodioecy. — Evolution. 10(2): 115–125. https://doi.org/10.1111/j.1558-5646.1956.tb02838.x
  38. Linnert G. 1958. Kerngesteuerte Gynodiözie bei Salvia nemorosa. — Z. Indukt. Abstamm. Vererbungsl. 89: 36–51. https://doi.org/10.1007/BF00888499
  39. Liu J., Li C.-Q., Dong Y., Yang X., Wang Y.-Z. 2018. Dosage imbalance of B- and C-class genes causes petaloid-stamen relating to F1 hybrid variation. — BMC Plant Biol. 18(1): 341. https://doi.org/10.1186/s12870-018-1562-4
  40. Lobo J.A., Ramos D.D.L., Braga A.C. 2016. Visitation rate of pollinators and nectar robbers to the flowers and inflorescences of Tabebuia aurea (Bignoniaceae): effects of floral display size and habitat fragmentation. — Bot. J. Linn. Soc. 181(4): 667–681. https://doi.org/10.1111/boj.12435
  41. McCauley D.E., Taylor D.R. 1997. Local population structure and sex ratio: evolution in gynodioecious plants. — Amer. Nat. 150(3): 406–420. https://doi.org/10.1086/286072
  42. Mucina L., Bültmann H., Dierßen K., Theurillat J.-P. et al. 2016. Vegetation of Europe: hierarchical floristic classification system of vascular plant, bryophyte, lichen, and algal communities. — Appl. Veg. Sci. 19(S1): 3–264. https://doi.org/10.1111/avsc.12257
  43. Müller H. 1873. Befruchtung der Blumen durch Insekten. Leipzig. 478 S.
  44. Naghiloo S., Claßen-Bockhoff R. 2016. Gradual inhibition of staminate structures results in various degrees of male sterility in Knautia arvensis. — Int. J. Plant Sci. 177(7): 608–617. https://doi.org/10.1086/687511
  45. Niu Y., Zhang Z.-Q., Liu C.-Q., Li Z.-M., Sun H. 2015. A sexually dimorphic corolla appendage affects pollen removal and floral longevity in gynodioecious Cyananthus delavayi (Campanulaceae). — PLoS ONE. 10(1): e0117149. https://doi.org/10.1371/journal.pone.0117149
  46. Oak M.K., Song J.H., Hong S.P. 2018. Sexual dimorphism in a gynodioecious species, Aruncus aethusifolius (Rosaceae). — Plant Syst. Evol. 304(4): 473–484. https://doi.org/10.1007/s00606-018-1493-4
  47. Oskay D. 2017. Reproductive biology of the critically endangered endemic plant Erodium somanum in Turkey. — Turk. J. Bot. 41(2): 171–179. https://doi.org/10.3906/bot-1603-9
  48. Plack A. 1957. Sexual dimorphism in Labiatae. — Nature. 180(4596): 1218–1219. https://doi.org/10.1038/1801218a0
  49. Ponomarev A.N., Demyanova E.I. 1975a. To the study of gynodioecy in plants. — Bot. Zhurn. 60(1): 3–15 (In Russ.).
  50. Ponomarev A.N., Demyanova E.I. 1975b. Nectar secretion in perfect and female flowers of gynodioecious plants. — Biol. nauki. 9: 67–72 (In Russ.).
  51. Ross M.D. 1969. Digenic inheritance of male sterility in Plantago lanceolata. — Can. J. Genet. Cytol. 11(3): 739–744. https://doi.org/10.1139/g69-086
  52. Schulz A. 1890. Beiträge zur Kenntniss der Bestäubungseinrichtungen und der Geschlechtsvertheilung bei den Pflanzen. II. — Bibl. Bot. 17: 1–224.
  53. Sletvold N., Agren J. 2016. Experimental reduction in interaction intensity strongly affects biotic selection. — Ecology. 97(11): 3091–3098. https://doi.org/10.1002/ecy.1554
  54. Sokal R.R., Rohlf F.J. 2012. Biometry: the principles and practice of statistics in biological research. 4th edition. New York. 937 p.
  55. Stanton M.L., Young H.J. 1994. Selection for floral character associations in wild radish, Raphanus sativus L. — J. Evol. Biol. 7(3): 271–285. https://doi.org/10.1046/j.1420-9101.1994.7030271.x
  56. Szabo Z. 1923. The development of the flower of the Dipsacaceae. — Ann. Bot. 37(146): 325–334. https://doi.org/10.1093/oxfordjournals.aob.a089848
  57. Taylor D.R., Olson M.S., McCauley D.E. 2001. A quantitative genetic analysis of nuclear-cytoplasmic male sterility in structured populations of Silene vulgaris. — Genetics. 158(2): 833–841. https://doi.org/10.1093/genetics/158.2.833
  58. Theißen G. 2001. Development of floral organ identity: stories from the MADS house. — Curr. Opin. Plant Biol. 4(1): 75–85. https://doi.org/10.1016/s1369-5266(00)00139-4
  59. Tsuji K., Ohgushi T. 2018. Florivory indirectly decreases the plant reproductive output through changes in pollinator attraction. — Ecol. Evol. 8(5): 2993–3001. https://doi.org/10.1002/ece3.3921
  60. Van Marrewijk G.A.M. 1969. Cytoplasmic male sterility in Petunia. I. Restoration of fertility with special reference to the influence of environment. — Euphytica. 18(1): 1–20. https://doi.org/10.1007/BF00021977
  61. Varga S., Soulsbury C.D., John E.A. 2022. Biological Flora of Britain and Ireland: Knautia arvensis. —
  62. J. Ecol. 110(8): 1970–1992. https://doi.org/10.1111/1365-2745.13938
  63. Wang H.-X., Liu H., Moore M.J., Landrein S., Liu B., Zhu Z.-H., Wang H.-F. 2020. Plastid phylogenomic insights into the evolution of the Caprifoliaceae s. l. (Dipsacales). — Molec. Phyl. Evol. 142: 106641. https://doi.org/10.1016/j.ympev.2019.106641

Supplementary files

Supplementary Files
Action
1. JATS XML
2. Fig. 1. Bisexual and pistillate flowers taking the marginal position in the cymoids of Knautia arvensis, in the plane of the first two principal components. X-axis — the first principal component, Y-axis — the second principal component. White squares — bisexual flowers, black circles — pistillate flowers.

Download (81KB)
3. Fig. 2. Bisexual and pistillate flowers taking the middle position in the cymoids of Knautia arvensis, in the plane of the first two principal components. X-axis — the first principal component, Y-axis — the second principal component. White squares — bisexual flowers, black circles — pistillate flowers.

Download (70KB)

Copyright (c) 2025 Russian Academy of Sciences