Outcrossing mating system in natural populations of the endangered aquatic fern Ceratopteris thalictroides in China as revealed by microsatellite markers: implications for conservation

Authors

  • Yuanhuo DONG Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Chengyu SONG Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Xueyi BAI Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Jie WEI Zhenxiong County Experimental Middle School, Zhaotong City, 657200 (CN)
  • Tingting NING Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Guoquan XU Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Hong LAN Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)
  • Kuo LIAO Chinese Academy of Sciences, Wuhan Botanical Garden, Key Laboratory of Aquatic Botany and Watershed Ecology, Wuhan, 430074 (CN)
  • Hong LIU South-Central University for Nationalities, College of Life Sciences, Wuhan, 430074 (CN)
  • Mengxue MA South-Central University for Nationalities, College of Life Sciences, Wuhan, 430074; Medical Branch, Huazhong University of Science & Technology Press, Wuhan, 430223 (CN)
  • Changli ZENG Jianghan University, College of Life Sciences, Hubei Engineering Research Center for Protection and Utilization of Special Biological Resources in the Hanjiang River Basin, Wuhan 430056 (CN)

DOI:

https://doi.org/10.15835/nbha52113386

Keywords:

Ceratopteris thalictroides, endangered fern, high outcrossing rate, outcrossing species, SSR

Abstract

In this study, the mating system of the endangered aquatic fern Ceratopteris thalictroides in China was investigated using microsatellite markers. The estimates of the multilocus outcrossing rate (tm) and single-locus outcrossing rate (ts) were high at the species level (tm = 0.701 and ts = 0.595, respectively), indicating that C. thalictroides is a predominantly outcrossing species. Negative F (inbreeding coefficient of the maternal parents) values (-0.137) at the species level indicated an excess of heterozygotes and low inbreeding in the populations analyzed. Our investigation revealed that some of the natural and ex situ conservation populations of C. thalictroides have a prolific capacity for vegetative growth. The results showed that the homosporous pteridophyte C. thalictroides in China predominantly favors gametophytic crossing with a certain level of inbreeding along with vegetative growth. Ten populations have been established for ex situ conservation in Wuhan, China, with a survival rate of more than 90%, and mature spores were collected from them. Several factors, including high dispersal of spores and gametophytes by flowing water, high gene flow, and the wide distribution of the species in China, with the occurrence of some large populations, may have resulted in a high outcrossing rate in Chinese C. thalictroides. The high outcrossing rate of C. thalictroides showed that ex situ plantings are most suitable for enhancing possible mixing of the different populations, thus minimizing inbreeding.

References

Adjie B, Masuyam S, Ishikawa H, Watano Y (2007). Independent origins of tetraploid cryptic species in the fern Ceratopteris thalictroides. Journal of Plant Research 120(1):129-138. https://doi.org/10.1007/s10265-006-0032-5

Adugna A, Sweeney PM, Bekele E (2013). Estimation of in situ mating systems in wild sorghum (Sorghum bicolor (L.) moench) in Ethiopia using SSR-based progeny array data: implications for the spread of crop genes into the wild. Journal of Genetics 92:3-10. http://dx.doi.org/10.1007/s12041-013-0214-6

An JC, Chang D, Bai SQ, Cheng ZH, Yan JJ, Zhang JB, … Qiu WJ (2021). Study on breeding strategies based on morphological characteristics and SSR markers of Saccharum arundinaceum. Acta Agrestia Sinica 4:813-820. https://doi.org/10.11733/j.issn.1007-0435.2021.04.023

Barrett SCH, Eckert CG (1990). Variation and evolution of mating systems in seed plants. In: Kawano S(Ed). Biological Approaches and Evolutionary Trends in Plants. Academic Press, San Diego, CA, pp 229-254.

Bartz M, Gola EM (2018). Meristem development and activity in gametophytes of the model fern, Ceratopteris richardii. Developmental Biology 444:107-115. https://doi.org/10.1016/j.ydbio.2018.10.005

Bora MS, Sarma KP (2021). Anatomical and ultrastructural alterations in Ceratopteris pteridoides under cadmium stress: A mechanism of cadmium tolerance. Ecotoxicology and Environmental Safety 218:112285. https://doi.org/10.1016/j.ecoenv.2021.112285

Calevo J, Gargiulo R, Bersweden L, Viruel J, Gonzalezonzález Montelongo C, Rebbas K, Fay MF (2021). Molecular evidence of species and subspecies level distinctions in the rare Orchis patens s.l. and implications for conservation. Biodiversity and Conservation 30:1293-1314. https://doi.org/10.1007/s10531-021-02142-6

Carey N, StrachanS R, Robson BJ (2018). Impacts of Indian waterfern (Ceratopteris thalictroides (L.) Brongn.) infestation and removal on macroinvertebrate biodiversity and conservation in spring‐fed streams in the Australian arid zone. Aquatic Conservation Marine and Freshwater Ecosystems 28:466-475. http://dx.doi.org/10.1002/aqc.2828

Chaix G, Gerber S, Razafimaharo V, Vigneron P, Verhaegen D, Hamon S (2003). Gene flow estimation with microsatellites in a Malagasy seed orchard of Eucalyptus grandis. Theoretical and Applied Genetics 107:705-712. https://doi.org/10.1007/s00122-003-1294-0

Chen GQ, Huang HW, Crawford DJ, Pan BR, Ge XJ (2009). Mating system and genetic diversity of a rare desert legume Ammopiptanthus nanus (Leguminosae). Journal of Systematics and Evolution 47:57-66. http://dx.doi.org/10.1111/j.1759-6831.2009.00003.x

Chen X, Chen Z, Huang W, Fu H, Cao J (2019). Proteomic analysis of gametophytic sex expression in the fern Ceratopteris thalictroides. Public Library of Science ONE 14(8):e0221470. https://doi.org/10.1371/journal.pone.0221470.

Conway SJ, Di Stilio VS (2020). An ontogenetic framework for functional studies in the model fern Ceratopteris richardii. Developmental Biology 457(1):20-29. https://doi.org/10.1016/j.ydbio.2019.08.017

Cook CDK (1990). Aquatic plant book. SPB Academic Publishing, Hague.

Dai JF, Yuan D, Zhang HJ (2020). Genetic diversity and mating system of seed orchard of Larix principis-rupprechtii based on SSR markers. The Journal of Hebei Forestry Science and Technology 4:7-11.

Dauphin B, Grant JR, Farrar DR (2020). Outcrossing mating system of the early-divergent moonwort fern (Botrychium lunaria, Ophioglossaceae) revealed in the European Alps, International Journal of Plant Sciences 181(9):926-936. https://doi.org/10.1086/710491

De Groot GA, Verduyn B, Wubs ERJ, Erkens RHJ, During HJ (2012). Inter-and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing. BMC Plant Biology 12:3. https://doi.org/10.1186/1471-2229-12-3

Diao ZS (1990). Aquatic weeds in China. Chongqing Press, Chongqing.

Dong X, Liao K., Hao F, Liu H, Qin R (2018b). Mating system and genetic variability of the endangered endemic aquatic Lycophyte, Isoetes yunguiensis, in China determined using AFLP markers. American Fern Journal 108(2):47-61.

Dong YH (2012). Habitat characteristics and community structure of Ceratopteris thalictroides at West Lake in Hangzhou. Hubei Agricultural Sciences 51(23):5381-5383.

Dong YH, Chen JM, Robert WG, Wang QF (2008). Genetic variation in the endangered aquatic fern Ceratopteris thalictroides (Parkeriaceae) in China: implications from RAPD and ISSR data for a conservation strategy. Botanical Journal of the Linnean Society 157:657-671. http://dx.doi.org/10.1111/j.1095-8339.2008.00836.x

Dong YH, Dai C, LiaoK (2013). Life form and community characteristics of the endangered aquatic fern Ceratopteris thalictroides at Taihu Lake in China: Implications for conservation strategies. Proceedings of 2013 International Conference on Frontiers of Environment, Energy and Bioscience (ICFEEB 2013). 2013:543-549.

Dong YH, Robert GW, Wang QF (2010). Genetic variation and gene flow in the endangered aquatic fern Ceratopteris pteridoides in China, and conservation implication. Annales Botanici Fennici 47:34-44. http://dx.doi.org/10.5735/085.047.0104

Dong ZR, Chen JM, Wang QF (2006). RAPD analysis for mating system in Caldesia parnassifolia. Journal of Wuhan Botanical Research 24:167-170.

Dong, Y.H., Robert, W.G., Chen, J.M., Wang, Q.F. (2005). Effect of habitat modification on the distribution of the endangered aquatic fern Ceratopteris thalictroides (Parkeriaceae) in China. Journal of Freshwater Ecology 20:689-693. http://dx.doi.org/10.1080/02705060.2005.9664792

Doyle JJ, Doyle JL (1987). A rapid DNA isolation method for small quantities of fresh tissues. Phytochemical Bulletin 19:11-15.

Fan JJ, Sheng JL, Li XH, Zhang XP (2018). Analysis on mating system of natural population of Pteroceltis tatarinowii based on SSR molecular marker. Journal of Plant Resources and Environment 27(4):110-112.

Fernando DD, Discenza JJ, Bouchard JR, Leopold DJ (2015). Genetic analysis of the threatened American hart's-tongue fern (Asplenium scolopendrium var. americanum [Fernald] Kartesz and Gandhi): Insights into its mating system and implications for conservation. Biochemical Systematics and Ecology 62:25-35. http://dx.doi.org/10.1016/j.bse.2015.07.034

Frankham R, Ballou JD, Briscoe DA (2002). Introduction to conservation genetics. Cambridge: Cambridge University Press.

Gaiotto FA, Bramucci M, Grattapaglia D (1997). Estimation of outcrossing rate in a breeding population of Eucalyptus urophylla with dominant RAPD and AFLP markers. Theoretical and Applied Genetics 95:842-849. https://doi.org/10.1007/s001220050634

Geng Y, Cai C, Mcadam SAM, Banks JA, Wisecaver JH, Zhou Y (2021). A De Novo transcriptome assembly of Ceratopteris richardii provides insights into the evolutionary dynamics of complex gene families in land plants. Genome Biology and Evolution 13(3). https://doi.org/10.1093/gbe/evab042

Guan BC, Liu X, Gong Xi, Cai QY, Ge G (2019). Genetic landscape and landscape connectivity of Ceratopteris thalictroides, an endangered aquatic fern. Ecological Informatics 53:100973. http://dx.doi.org/10.1111/j.1095-8339.2008.00836.x

Han YC, Teng CZ, Wahiti GR, Zhou MQ, Hu ZL, Song YC (2009). Mating system and genetic diversity in natural populations of Nelumbo nucifera (Nelumbonaceae) detected by ISSR markers. Plant Systematics and Evolution 277:13-20. http://dx.doi.org/10.1007/s00606-008-0096-x

Haufler CH, Pryer KM, Schuettpelz E, Sessa EB, Farrar DR, Moran R, ... Windham MD (2016). Sex and the single gametophyte: Revising the homosporous vascular plant life cycle in light of contemporary research. Bioscience 66(11):928-37. https://doi.org/10.1093/biosci/biw108

Heike L, Dagmar S (2022). Flowering behavior of clones in a Norway maple (Acer platanoides) seed orchard and mating system analysis using nuclear SSR markers. European Journal of Forest Research 141(4):561-569. https://doi.org/10.1007/s10342-022-01459-3

Hickok LG, Warne TR, Fribourg RS (1995). The biology of the fern Ceratopteris and its use as a model system. International Journal of Molecular Sciences 156:332-345. http://dx.doi.org/10.1086/297255

Innes J, Hermanutz IA (1998). The mating system and genetic structure in a disjunct population of the seaside goldenrod Solidago sempervirens L. (Asteraceae). Heredity 61:447-454. https://doi.org/10.1038/hdy.1988.137

Kinosian SP, Pearse WD, Wolf PG (2020). Cryptic diversity in the model fern genus Ceratopteris (Pteridaceae), Molecular Phylogenetics and Evolution. https://doi.org/10.1016/j.ympev.2020.106938

Krauss SL, Hood P, Zawko G, Mattner J (2000). Recent advances and new genetic tools for the delineation of provenances. In: Asher CJ, Bell LC (Eds). Proceedings of the third Australian workshop on native seed biology for revegetation. Brisbane: Australian Centre for Mining Environmental Research, pp 13-23.

Liao YY, Yang XY, Motley TJ, Chen JM, Wang QF (2011). Phylogeographic analysis reveals two cryptic species of the endangered fern Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae) in China. Conservation Genetics 12:1357-1365. http://dx.doi.org/10.1007/s10592-011-0236-7

Lloyd RM (1974a). Systematics of the genus Ceratopteris Brongn. (Parkeriaceae) II. Taxonomy. Brittonia 26:139-160. https://doi.org/10.2307/2805883

Lloyd RM (1974b). Reproductive biology and evolution in the Pteridophyta. Annals of the Missouri Botanical Garden 61:318-331. https://doi.org/10.2307/2395060

Lott MS, Volin JC, Pemberton RW, Austin DF (2003). The reproductive biology of the invasive ferns Lygodium microphyllum and L. japonicum (Schizaeaceae): implications for invasive potential. American Journal of Botany 90:1144-1152. http://dx.doi.org/10.3732/ajb.90.8.1144

Lu WX, Zou Z, Hu XY, Yang SC (2022). Genetic diversity and mating system of two mangrove species (Rhizophora apiculata and Avicennia marina) in a heavily disturbed area of China. Diversity 14(2):115. https://doi.org/10.3390/d14020115

Masuyama S, Watano Y (1990). Trends for inbreeding in polyploid pteriodphytes. Plant Species Biology 5:13-17. https://doi.org/10.1111/j.1442-1984.1990.tb00188.x

Masuyama S, Watano Y (2010). Cryptic species in the fern Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae). IV. Taxonomic revision. Acta Phytotaxonomica Et Geobotanica 61(2):75-86. http://dx.doi.org/10.18942/apg.KJ00009281704

Masuyama S, Yatabe Y, Murakami N, Watano Y (2002). Cryptic species in the fern Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae). I. Molecular analyses and crossing tests. Journal of Plant Research 115:87-97. https://doi.org/10.1007/s102650200013

Maunder M (1994). Botanical gardens: future challenges and responsibilities. Biodiversity and Conservation 3:97-103.

National Forestry and Grassland Administration, PRC (2021). Announcement of the National Forestry and Grassland Administration, PRC and Ministry of Agriculture and Rural Affairs, PRC (No. 15 of 2021) (List of National Key Protected Wild Plants). http://www.forestry.gov.cn/2021-09-08

Pelosi J, Sessa EB (2021). From genomes to populations: A meta-analysis and review of fern population genetics. International Journal of Plant Sciences 182(5). https://doi.org/10.1086/713442

Pickup M, Brandvain Y, Frasse C, Yakimowski S, Barton NH, Dixit T, Field DL (2019). Mating system variation in hybrid zones: facilitation, barriers and asymmetries to gene flow. New Phytologist 224:1035-1047. https://doi.org/10.1111/nph.16180

Pometti CL, Bessega CF, Vilardi JC, Saidman BO (2013). Comparison of mating system parameters and genetic structure in three natural scenarios of Acacia visco (Leguminosae, Mimosoideae). Plant Systematics and Evolution 299:761-771.

PPGI (2016). A community-derived classification for extant lycophytes and ferns. Journal of Systematics and Evolution 54:563-603. https://doi.org/10.1111/jse.12229

Primack RB (1993). Essentials of conservation biology. Sinauer Associates, Inc, Sunderland, MA

Qi XQ, Ge YF, Li DW (2016). Molecular clone and sequence analysis of hemoglobin gene in Ceratopteris thalictroides. Guihaia 36(2):216-223.

Qian W, Ge S, Hong DY (2001). Genetic variation within and among populations of a wild rice Oryza granulata from China detected by RAPD and ISSR markers. Theoretical and Applied Genetics 102:440-449. https://doi.org/10.1007/s001220051665

Raju VS (1983). Ceratopteris thalictroides (L.) Brongn. (Parkeriaceae) from the Godavari region of Andhra Pradesh. Journal of Economic and Taxonomic Botany 4:316.

Ranker TA, Houston HA (2002). Is gametophyte sexuality in the laboratory a good predictor of sexuality in nature? American Fern Journal 92:112-118. http://dx.doi.org/10.1640/0002-8444(2002)092[0112:IGSITL]2.0.CO;2

Ritland K (1990). A series of FORTRAN computer programs for estimating plant mating systems. Journal of Heredity 81:235-237. https://doi.org/10.1093/oxfordjournals.jhered.a110982

Ritland K (2009). Multilocus mating system program MLTR. Version 3.4. University of British Columbia, Canada. Available at: http://genetics.forestry.ubc.ca/ritland/programs.html

Ritland K, Jain S (1981). A model for the estimation of outcrossing rate and gene frequencies using n independent loci. Heredity 47:35-52. https://doi.org/10.1038/hdy.1981.57

Ritland K (2002). Extensions of models for the estimation of mating systems using n independent loci. Heredity 88:221-228. https://doi.org/10.1038/sj.hdy.6800029

Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998). Inbreeding and extinction in a butterfly metapopulation. Nature 392:491-494. http://dx.doi.org/10.1038/33136

Saki S, Bagheri H, Deljou A, Zeinalabedini M (2016). Evaluation of genetic diversity amongst Descurainia sophia L. genotypes by inter-simple sequence repeat (ISSR) marker. Physiology and Molecular Biology of Plants: An International Journal of Functional Plant Biology 22:97-105. https://doi.org/10.1007/s12298-015-0330-2

Santos-Garcia MO, Resende RMS, Chiari L, Zucchi MI, Souza AP (2010). Mating systems in tropical forages: Stylosanthes capitata Vog. and Stylosanthes guianensis (Aubl.) Sw. Euphytica. https://doi.org/10.1007/s10681-010-0293-x

Schedlbauer MD, Klekowski EJ (1972). Antheridiogen actvity in the fern Ceratopteris thalictroides (L.) Brongn. Botanical Journal of the Linnean Society 56:339-413.

Sharma SS, Islam MA, Negi MS Tripathi SB (2017). Estimation of outcrossing rates in biodiesel species Pongamia pinnata based on AFLP and microsatellite markers. National Academy Science Letters 40(2):105-108. http://dx.doi.org/10.1007/s40009-016-0533-2

Sinha P, Islam MA, Negi MS, Tripathi SB (2015). Estimation of outcrossing rates in interspecific backcross plants of Jatropha curcas (L.) using AFLP and SSR markers. Physiology and Molecular Biology of Plants 21(4):605-609. https://doi.org/10.1007%2Fs12298-015-0318-y

Soltis DE, Soltis PS (1992). The distribution of selfing rates in homosporous ferns. American Fern Journal 79:97-100. https://doi.org/10.2307/2445202

Soltis PS, Soltis DE (1990a). Genetic variation within and among populations of ferns. American Fern Journal 80:161-172. https://doi.org/10.2307/1547205

Soltis PS, Soltis DE (1990b). Evolution of inbreeding and outcrossing in ferns and fern-allies. Plant Species Biology 5:1-11. http://dx.doi.org/10.1111/j.1442-1984.1990.tb00187.x

Sun XH, Wang F, Cui R, Liu X, Li XX, Dong JB, Sun L, Qin SQ, Wang RQ, Zheng PM, Wang H (2020). Studies on reproductive strategies of Vitex negundo L. var. heterophylla (Franch.) Rehder (Lamiaceae) based on morphological characteristics and SSR markers. Ecology and Evolution. https://doi.org/10.1002/ece3.6271

Suwarni E, Omondi SF, Dancik BP, Khasa DP (2018). Estimation of pollen contamination and mating system in Pinus merkusii seedling seed orchard using allozyme markers. Journal of Tropical Forest Science 30:95-105.

Tang JM (2014). Studies on mating system of Camellia tunghinensis Chang based on SSR markers and its drought resistance. Guangxi Normal University.

Torres Carbonell F, Ureta S, Pandolfo C, Presotto A (2020). Molecular characterization of imidazolinone-resistant Brassica rapa × B. napus hybrids. Environmental Monitoring and Assessment 192:746, https://doi.org/10.1007/s10661-020-08711-6

Warne T, Hickok L (1987). (2-Chloroethyl) phosphoric acid promotes germination of immature spores of Ceratopteris richardii Brongn. Plant Physiology 83:723-725. https://doi.org/10.1104/pp.83.4.723

Watano Y, Masuyama S (1991). Inbreeding in natural populations of the annual polyploidy fern Ceratopteris thalictroides (Parkeriaceae). Systematic Botany 16:705-714. https://doi.org/10.2307/2418872

Watano Y, Masuyama S (1994). Genetic differentiation in populations of the polymorphic fern Ceratopteris thalictroides in Japan. Journal of Plant Research 107:139-146. https://doi.org/10.1007/BF02346009

Wright S (1965). The interpretation of population structure by F2 statistics with special regard to systems of mating. Evolution 19:395-420. https://doi.org/10.2307/2406450

Wubs ERJ, Groot GAD, During HJ, Vogel JC, Grundmann M, Bremer P, Schneider H (2010). Mixed mating system in the fern Asplenium scolopendrium: implications for colonization potential. Annals of Botany (Oxford) 106:583-590. https://doi.org/10.1093/aob/mcq157

Yang XY, Long ZC, Gichira AW, Guo YH, Wang QF, Chen JM (2016). Development of microsatellite markers in the tetraploid fern Ceratopteris thalictroides (Parkeriaceae) using RAD tag sequencing. Genetics and Molecular Research 15(1). https://doi.org/10.4238/gmr.15017550.

Yu YF (1999). A milestone of wild plant conservation in China. Plants 5:3-11.

Zhang R, Wang FG, Zhang J, Shang H, Liu L, Wang H, ... Yan YH (2019). Dating whole genome duplication in Ceratopteris thalictroides and potential adaptive values of retained gene duplicates. International Journal of Molecular Sciences 20:1926. https://doi.org/10.3390/ijms20081926

Zhang R, Yu JH, Shao W, Wang WQ, Yan YH (2020). Ceratopteris shingii, a new species of Ceratopteris with creeping rhizomes from Hainan, China. Phytotaxa 449:23-30. https://doi.org/10.11646/phytotaxa.449.1.323

Zhang ZJ, Meng JX, Pan DF, Yang C, Li Y (2018). Mating system and progeny genetic diversity of Camellia oleifera‘Ruan Zhi’. Journal of Forestry Research. https://doi.org/10.1007/s11676-018-0732-4

Zhao HB, Zhou LH, Liu HH, Bao ZY (2014). Genetic effects of different mating modes in Sinocalycanthus chinensis (Cheng et S.Y. Chang) Cheng et S.Y. Chang, an endangered species endemic to Zhejiang Province, China. Biochemical Systematics and Ecology 54:8-14. http://dx.doi.org/10.1016/j.bse.2013.12.021

Downloads

Published

2024-03-11

How to Cite

DONG, Y., SONG, C., BAI, X., WEI, J., NING, T., XU, G., LAN, H., LIAO, K., LIU, H., MA, M., & ZENG, C. (2024). Outcrossing mating system in natural populations of the endangered aquatic fern Ceratopteris thalictroides in China as revealed by microsatellite markers: implications for conservation. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 52(1), 13386. https://doi.org/10.15835/nbha52113386

Issue

Section

Research Articles
CITATION
DOI: 10.15835/nbha52113386