Genetic diversity of the critically endangered Ferula sinkiangensis K.M.Shen (Apiaceae) and the implications for conservation

Genetic diversity of the critically endangered Ferula sinkiangensis K.M.Shen (Apiaceae) and the implications for conservation

Research on the genetic diversity and structures of endangered plant species with small population sizes is a prerequisitefor developing reasonable conservation strategies. Ferula sinkiangensis K.M.Shen is a critically endangered herbaceous perennial andmonocarpic medical plant growing in semiarid steppe ecosystems with a small population size within the Yili Valley in Xinjiang, China.Unfortunately, the lack of genetic information has limited our ability to initiate effective conservation strategies for the species. In thisstudy, 14 polymorphic microsatellite primers of F. sinkiangensis were developed and characterized using Illumina HiSeq paired-endreads from genomic DNA. Primers were used to assess the genetic diversity and structure of the species in the Yili Valley. A total of 92alleles were detected across 14 microsatellite loci from 65 specimens of F. sinkiangensis. Moderate to high levels of genetic diversity (He= 0.446, I = 0.821, PPB = 92.86%) were found within the species. Our results contradict the general hypothesis that rare and endangeredspecies with small population sizes and narrow ranges of distribution exhibit low levels of genetic diversity. The moderate to high levelsof genetic diversity within the species can be explained by the mating system, life history traits, and human activities in recent years.Several reasonable conservation and reintroduction strategies are proposed, including maintenance of the plant’s natural habitats, seedsor seedlings collection for germplasm storage, and artificial breeding of the species.

___

  • Allendorf FW, Luikart G, Aitken SN (2013). Conservation and the Genetics of Populations, 2nd Ed. Hoboken, NJ, USA: WileyBlackwell.
  • Bilgen BB, Barut AK, Demirbaş S (2019). Genetic characterization of Orobanche cumana populations from the Trace region of Turkey using microsatellite markers. Turkish Journal of Botany 43: 38-47.
  • Chiang YC, Hung KH, Schaal BA, Ge XJ, Hsu TW et al. (2006). Contrasting phylogeographical patterns between mainland and island taxa of the Pinus luchuensis complex. Molecular Ecology 15: 765-779.
  • Cornuet JM, Luikart G (1996). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144: 2001-2014.
  • Darwin C (1859). The Origin of Species. London, UK: John Murry. Dettori CA, Loi MC, Brullo S, Arguimbau PF, Tamburini E et al. (2016). The genetic diversity and structure of the Ferula communis L. complex (Apiaceae) in the Tyrrhenian area. Flora 223: 138-146.
  • Dettori CA, Sergi S, Tamburini E, Bacchetta G (2013). The genetic diversity and spatial genetic structure of the Corso-Sardinian endemic Ferula arrigonii Bocchieri (Apiaceae). Plant Biology 16: 1005-1013.
  • Dong YH, Chen JM, Gituru RW, Wang QF (2007). Gene flow in populations of the endangered aquatic fern Ceratopteris pteridoides in China as revealed by ISSR markers. Aquatic Botany 87: 69-74.
  • Feng L, Xu ZY, Wang L (2019). Genetic diversity and demographic analysis of an endangered tree species Diplopanax stachyanthus in subtropical China: implications for conservation and management. Conservation Genetics 20: 315-327.
  • Flight PA (2010). Phylogenetic comparative methods strengthen evidence for reduced genetic diversity among endangered tetrapods. Conservation Biology 24: 1307-1315.
  • Frankham R (1997). Do island populations have less genetic variation than mainland populations? Heredity 78: 311-327.
  • Frankham R, Ballou JD, Briscoe DA (2002). Introduction to Conservation Genetics. Cambridge, UK: Cambridge University Press.
  • Frankham R, Ballou JD, Ralls K, Eldridge M, Dudash MR et al. (2017). Genetic Management of Fragmented Animal and Plant Populations. Oxford, UK: Oxford University Press.
  • Gordon SP, Sloop CM, Davis HG, Cushman JH (2012). Population genetic diversity and structure of two rare vernal pool grasses in central California. Conservation Genetics 13: 117-130.
  • Goudet J (1995). FSTAT (version 1.2): A computer program to calculate F-statistics. Journal of Heredity 86: 485-486.
  • Hamrick JL, Godt MJW (1989). Allozyme diversity in plant species. In: Brown HD, Clegg MT, Kahler AL (editors). Plant Population Genetics, Breeding and Genetic Resources. Sunderland, MA, USA: Sinauer Associates, Inc., pp. 43-46.
  • Hamrick JL, Godt MJ (1996). Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society B 351: 1291-1298.
  • Hamrick JL, Godt MJW, Sherman-Bryoles SL (1992). Factors influencing levels of genetic diversity in woody plant species. New Forests 6: 95-124
  • Huang LQ, Xiao PG, Wang YY (2012). Investigation on Rare and Endangered Medicinal Plant Resources in China. Shanghai, China: Science and Technology Press (in Chinese).
  • Kalinowski ST, Taper ML, Marshall TC (2007). Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Molecular Ecology 16: 1099-1106.
  • Koul P, Sharma N, Koul AK (1993). Pollination biology of Apiaceae. Current Science 65: 219-222.
  • Leimu R, Mutikaninen P, Koricheva J, Fischer M (2006). How general are positive relationships between plant population size, fitness and genetic variation? Journal of Ecology 94: 942-952.
  • Li WJ, Su ZH, Li AR, Guan KY, Feng Y (2019). Isolation and characterization of 18 microsatellites for the invasive native Pedicularis kansuensis (Orobanchaceae). Grassland Science 65: 135-138.
  • Li ZZ, Lu MX, Gichira AW, Islam MR, Wang QF et al. (2019). Genetic diversity and population structure of Ottelia acuminata var. jingxiensis, an endangered endemic aquatic plant from southwest China. Aquatic Botany 152: 20-26.
  • Loveless MD, Hamrick JL (1984). Ecological determinants of genetic structure of plant populations. Annual Review of Ecology, Evolution, and Systematics 15: 65-95.
  • Luan SS, Chiang TY, Gong X (2006). High genetic diversity vs. low genetic differentiation in Nouelia insignis (Asteraceae), a narrowly distributed and endemic species in China, revealed by ISSR fingerprinting. Annals of Botany 98: 583-589.
  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998). Distortion of allele frequency distributions provides a test for recent population bottlenecks. Journal of Heredity 89: 238- 247.
  • Mahendra P, Bisht S (2012). Ferula asafoetida: Traditional uses and pharmacological activity. Pharmacognosy Reviews 6: 141- 146.
  • Markert JA, Champlin DM, Gutjahr-Gobell R, Grear JS, Kuhn A et al. (2010). Population genetic diversity and fitness in multiple environments. BMC Evolutionary Biology 10: 205.
  • Meloni M, Reid A, Caujapé-Castells J, Soto M, María J et al. (2015). High genetic diversity and population structure in the endangered Canarian endemic Ruta oreojasme (Rutaceae). Genetica 143: 571-580.
  • Nei M, Maruyama T, Chakraborty R (1975). The bottleneck effect and genetic variability in populations. Evolution 29: 1-10.
  • Nisar M, Khan A, Wadood SF, Shah AA, Hanci F (2017). Molecular characterization of edible pea through EST-SSR markers. Turkish Journal of Botany 41: 338-346.
  • Nybom H (2004). Comparison of different nuclear DNA markers for estimating intraspecific genetic diversity in plants. Molecular Ecology 13: 1143-1150.
  • Ottewell KM, Bickerton DC, Byrne M, Lowe AJ (2015). Bridging the gap: a genetic assessment framework for population-level threatened plant conservation prioritization and decisionmaking. Diversity and Distributions 22: 174-188.
  • Palsbøll PJ, Bérubé M, Allendorf FW (2007). Identification of management units using population genetic data. Trends in Ecology & Evolution 22: 11-16.
  • Peakall R, Smouse PE (2012). GenAlEx 6.5: Genetic Analysis in Excel. Population genetic software for teaching and research - an update. Bioinformatics 28: 2537-2539.
  • Pérez-Collazos E, Catalań P (2008). Conservation genetics of the endangered Iberian steppe plant Ferula loscosii (Apiaceae). Plant Biology 10: 492-501.
  • Pimenov MG, Leonov MV (1993). The Genera of the Umbelliferae. Kew, UK: Royal Botanic Gardens.
  • Piry S, Luikart G, Cornuet JM (1999). BOTTLENECK: A computer program for detecting recent reductions in the effective population size using allele frequency data. Journal of Heredity 90: 502-503.
  • Qiao Q, Zhang CQ, Milne RI (2010). Population genetics and breeding system of Tupistra pingbianensis (Liliaceae), a naturally rare plant endemic to SW China. Journal of Systematics and Evolution 48: 47-57.
  • Qin HN, Yang Y, Dong SY, He Q, Jia Y et al. (2017). Threatened species list of China’s higher plants. Biodiversity Science 25 (7): 696-744 (in Chinese with an abstract in English).
  • Rahali FZ, Lamine M, Gargouri M, Rebey IB, Hammami M et al. (2016). Metabolite profiles of essential oils and molecular markers analysis to explore the biodiversity of Ferula communis: towards conservation of the endemic giant fennel. Phytochemistry 124: 58-67.
  • Raymond M, Rousset F (1995). GENEPOP (version 1.2): Population genetics software for exact tests and ecumenicism. Journal of Heredity 86: 248-249.
  • Rousset F (2008). Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Molecular Ecology Resources 8: 103-106.
  • Rozen S, Skaletsky HJ (2000). Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (editors). Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, NJ, USA: Humana Press.
  • Schou M, Loeschcke V, Bechsgaard J, Schlotterer C, Kristensen T (2017). Unexpected high genetic diversity in small populations by associative overdominance. Molecular Ecology 26: 6510-6523.
  • Schuelke M (2000). An economic method for the fluorescent labeling of PCR fragments. Nature Biotechnology 18: 233-234.
  • She ML, Watson MF (2005). Ferula L. In: Wu ZY, Raven PH, Hong DY (editors). Flora of China, Volume 14. Beijing, China: Science Press: St. Louis, MO, USA: Missouri Botanical Garden Press. Shen GM (1987). Ferula L. Urumqi, China: Volksverlag Xinjiang (in Chinese).
  • Shen GM, Ramil, Yang G, Xu LR (1975). Two new species of Ferula and their economical significances in Sinkiang. Acta Phytotaxonomica Sinica 13: 88-92 (in Chinese with an abstract in English).
  • Shiga T, Yokogawa M, Kaneko S, Isagi Y (2017). Genetic diversity and population structure of Nuphar submerse (Nymphaeaceae), a critically endangered aquatic plant endemic to Japan, and implications for its conservation. Journal of Plant Research 130: 83-93.
  • Tajbakht P, Talebi M, Rahimmalek M (2018). Genetic diversity among and within Ferula asafoetida H. Karst. Populations using molecular and phytochemical markers. Phytochemistry 155: 19-29.
  • Vieira ÂF, Dias EF, Moura M (2018). Geography, geology and ecology influence population genetic diversity and structure in the endangered endemic Azorean Ammi (Apiaceae). Plant Systematics and Evolution 304: 163-176.
  • Wang S, Xie Y (2004). Chinese Species Red List (Vol. 1). Beijing, China: Higher Education Press (in Chinese).
  • Wu FQ, Shen SK, Zhang XJ, Wang YH, Sun WB (2015). Genetic diversity and population structure of an extremely endangered species: the world’s largest Rhododendron. AoB Plants 7: plu082. doi: 10.1093/aobpla/plu082
  • Yamashiro T, Yamashiro A, Inoue M, Maki M (2016). Genetic diversity and divergence in populations of the threatened grassland perennial Vincetoxicum atratum (ApocynaceaeAsclepiadoideae) in Japan. Journal of Heredity 107: 455-462.
  • Yang J, Zhao LL, Yang JB, Sun WB (2015). Genetic diversity and conservation evaluation of a critically endangered endemic maple, Acer yangbiense, analyzed using microsatellite markers. Biochemical Systematics and Ecology 60: 193-198.
  • Yaqoob U, Nawchoo IA (2016). Reproductive ecology of an endangered monocarpic herbaceous perennial, Ferula jaeschkeana Vatke. Tropical Ecology 57: 849-864.
  • Young A, Boyle T, Brown T (1996). The population genetic consequences of habitat fragmentation for plants. Trends in Ecology & Evolution 11: 413-418.
  • Zawko G, Krauss SL, Dixon KW, Sivasithamparam K (2001). Conservation genetics of the rare and endangered Leucopogon obtectus (Ericaceae). Molecular Ecology 10: 2389-2396.
  • Zhang LJ, Sun XB, Si JY, Li GZ, Cao L (2019). Umbelliprenin isolated from Ferula sinkiangensis inhibits tumor growth and migration through the disturbance of Wnt signaling pathway in gastric cancer. PLoS One 14: e0207169. doi: 10.1371/journal. pone.0207169
  • Zhou XJ, Ren XL, Liu WZ (2016). Genetic diversity of SSR markers in wild populations of Tapiscia sinensis, an endangered tree species. Biochemical Systematics and Ecology 69: 1-5.