Effects of symbiotic fungi on seed germination of interspecific hybrid progenies in Orchidaceae

doi:10.17521/cjpe.2019.0048

Abstract

Abstract:

AimsPrevious studies have shown that Dendrobium plants form a specific symbiotic relationship with fungi at differentiation stages during natural seed germination. In order to explore the evolution and adaptation of this symbiotic relationship in interspecific hybrid progenies, this study was to understand whether the strong specificity with symbiotic fungi during seedling formation and differentiation was also an important factor limiting the formation of hybrid progenies in Dendrobium, and the relationship between hybrid progenies of orchids and symbiotic fungi during seed germination stage.
MethodsThe effects of fungi on germination of interspecific hybrid seeds of D. officinale and D. tortile were studied using the highly specific fungi strains Tulasnella SSCDO-5 and Epulorhiza FDd1, which can effectively promote seed germination and seedling formation in D. officinale and D. devonianum, respectively.
Important findings The results showed that both SSCDO-5 and FDd1 strains could effectively promote the protocorm and seedling formation of hybrid seeds after 68 days incubation with no significant difference. The SSCDO-5 strain from D. officinale did not show any advantages, and the seedling formation rate of hybrid was lower than that of FDd1 strain from D. devonianum. The seedling formation rate incubation with SSCDO-5 strain was (22.13 ± 6.62)% while with FDd1 strain was (29.53 ± 5.51)%. The specificity of SSCDO-5 strain with D. officinale at seedling formation and development stage was not inherited or expressed in hybrid progenies, indicating that hybridization broke the symbiotic relationship of this specificity, which enabled hybrid progenies to establish new symbiotic relationship with different fungi. Our results do not support the hypothesis that the specificity of symbiotic fungi is an important limiting factor for the formation of hybrid progenies in Dendrobium. We speculate that the symbiotic relationship between Dendrobium plants and fungi during seedling differentiation and development is formed and established in the process of adapting to specific ecological environment.

http://jtp.cnki.net/bilingual/detail/html/ZWSB201904010

Key words: symbiosis specificity, mycorrhizal fungi, Orchidaceae, Dendrobium, hybrid speciation, symbiotic seed germination

FAN Zi-Teng, WU Yu-Ling, WANG Xin-Ju, LI Tai-Qiang, GAO Jiang-Yun. Effects of symbiotic fungi on seed germination of interspecific hybrid progenies in Orchidaceae[J]. Chin J Plant Ecol, 2019, 43(4): 374-382.

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Figures/Tables 3

References 43

[1]	Aceto S, Caputo P, Cozzolino S, Gaudio L, Moretti A ( 1999). Phylogeny and evolution of Orchis and allied genera based on ITS DNA variation: Morphological gaps and molecular continuity. Molecular Phylogenetics & Evolution, 13, 67-76.
[2]	Arditti J ( 1967). Factors affecting the germination of orchid seeds. The Botanical Review, 33, 1-97.
[3]	Arditti J, Ghani AKA ( 2000). Numerical and physical properties of orchid seeds and their biological implications. New Phytologist, 145, 367-421.
[4]	Bidartondo MI, Read DJ (2008). Fungal specificity bottlenecks during orchid germination and development. Molecular Ecology, 17, 3707-3716.
[5]	Brundrett MC, Scade A, Batty AL, Dixon KW, Sivasithamparam K ( 2003). Development of in situ and ex situ seed baiting techniques to detect mycorrhizal fungi from terrestrial orchid habitats. Mycological Research, 107, 1210-1220.
[6]	Chase MW, Cameron KM, Freudenstein JV, Pridgeon AM, Salazar G, Berg C, Schuiteman A ( 2015). An updated classification of Orchidaceae. Botanical Journal of the Linnean Society, 177, 151-174.
[7]	Coyne JA, Orr HA ( 2004). Speciation. Sinauer Associates, Sunderland, USA.
[8]	Cozzolino S, Widmer A ( 2005). Orchid diversity: An evolutionary consequence of deception? Trends in Ecology & Evolution, 20, 487-494.
[9]	Dafni A, Ivri Y (1979). Pollination ecology of, and hybridization between,Orchis coriophora L. and O. collina Sol. ex Russ.(Orchidaceae) in Israel. New Phytologist, 83, 181-187.
[10]	Dearnaley JDW, Martos F, Selosse MA (2012). Orchid mycorrhizas: Molecular ecology, physiology, evolution and conservation aspects. In: Hock B ed. Fungal Associations. 2nd edn. Springer, Berlin,Germany. 207-230.
[11]	Dearnaley JWD, Perotto S, Selosse MA (2016). Structure and development of orchid mycorrhizas. In: Martin F ed. Molecular Mycorrhizal Symbiosis. Springer, Berlin. 63-86.
[12]	Gao JY, Liu Q, Yu DL (2014). Orchids of Xishuangbanna: Diversity and Conservation. China Forestry Publishing House, Beijing. 15-31.
	[ 高江云, 刘强, 余东莉 (2014). 西双版纳的兰科植物: 多样性和保护. 中国林业出版社, 北京. 15-31.]
[13]	Hegarty MJ, Hiscock SJ ( 2005). Hybrid speciation in plants: New insights from molecular studies. New Phytologist, 165, 411-423.
[14]	Hollick PS, Taylor RJ, McComb JA, Dixon KW ( 2005). If orchid mycorrhizal fungi are so specific, how do natural hybrids cope? Selbyana, 26, 159-170.
[15]	Huang H, Zi XM, Lin H, Gao JY ( 2018). Host-specificity of symbiotic mycorrhizal fungi for enhancing seed germination, protocorm formation and seedling development of over-collected medicinal orchid,Dendrobium devonianum. Journal of Microbiology, 56, 42-48.
[16]	Kauth P, Dutra D, Johnson T (2008). Techniques and applications of in vitro orchid seed germination. In: Teixeira da Silva JA ed. Floriculture, Ornamental and Plant Biotechnology: Advances and Topical Issues. Global Science Books, Iselworth,UK. 375-391.
[17]	Lee YI ( 2007). The asymbiotic seed germination of six Paphiopedilum species in relation to the time of seed collection and seed pretreatment. Acta Horticulturae, 755, 381-386.
[18]	Liu HX, Luo YB, Liu H ( 2010). Studies of mycorrhizal fungi of Chinese orchids and their role in orchid conservation in China―A review. The Botanic Review, 76, 241-262.
[19]	Long B, Niemiera AX, Cheng ZY, Long CL ( 2010). In vitro propagation of four threatened Paphiopedilum species (Orchidaceae). Plant Cell Tissue and Organ Culture, 101, 151-162.
[20]	Mallet J ( 2005). Hybridization as an invasion of the genome. Trends in Ecology & Evolution, 20, 229-237.
[21]	Martos F, Francios M, Pailler T, Kottke I, Cédric G, Marc- André Selosse ( 2012). The role of epiphytism in architecture and evolutionary constraint within mycorrhizal networks of tropical orchids. Molecular Ecology, 21, 5098-5109.
[22]	Masuhara G, Katsuya K (1994). In situ and in vitro specificity between Rhizoctonia spp. and Spiranthes sinensis(Persoon) Ames. var. amoena 127, 711-718.
[23]	McCormick MK, Jacquemyn H ( 2014). What constrains the distribution of orchid populations? New Phytologist, 202, 392-400.
[24]	McKendrick SL, Leake JR, Read DJ ( 2000). Symbiotic germination and development of myco-heterotrophic plants in nature: Transfer of carbon from ectomycorrhizal Salix repens and Betula pendula to the orchid Corallorhiza trifida through shared hyphal connections. New Phytologist, 145, 539-548.
[25]	Meng YY, Shao SC, Liu SJ, Gao JY ( 2019). Do the fungi associated with roots of adult plants support seed germination? A case study on Dendrobium exile(Orchidaceae). Global Ecology and Conservation, 17, e00582. DOI: 10.1016/‍ j.gecco.2019.e00582.
[26]	Nontachaiyapoom S, Sasirat S, Manoch L ( 2010). Isolation and identification of Rhizoctonia-like fungi from roots of three orchid genera, Paphiopedilum, Dendrobium, and Cymbidium, collected in Chiang Rai and Chiang Mai provinces of Thailand. Mycorrhiza, 20, 459-471.
[27]	Ramsay MM, Stewart J ( 1998). Re-establishment of the lady’s slipper orchid (Cypripedium Calceolus L.) in Britain. Botanical Journal of the Linnean Society, 126, 173-181.
[28]	Rasmussen HN, Dixon KW, Jersakova J, Tesitelova T ( 2015). Germination and seedling establishment in orchids: A complex of requirements. Annals of Botany, 116, 391-402.
[29]	Roberts DL (2003). Pollination biology: The role of sexual reproduction in orchid conservation. In: Dixon KW, Kell SP, Barrett RL, Cribb PJ eds. Orchid Conservation. Natural History Publications, Kota Kinabalu, Sabah. 113-136.
[30]	Schatz B ( 2006). Fine scale distribution of pollinator explains the occurrence of the natural orchid hybrid × Orchis bergonii. Ecoscience, 13, 111-118.
[31]	Schatz B, Geoffroy A, Dainat B, Bessiere JM, Buatois B, Hossaert-Mckey M, Selosse MA ( 2010). A case study of modified interactions with symbionts in a hybrid mediterranean orchid. American Journal of Botany, 97, 1278-1288.
[32]	Sheng CL, Li YY, Gao JY ( 2012). Ex situ symbiotic seed germination, isolation and identification of effective symbiotic fungus in Cymbidium mannii(Orchidaceae). Chinese Journal of Plant Ecology, 36, 859-869.
	[ 盛春玲, 李勇毅, 高江云 ( 2012). 硬叶兰种子的迁地共生萌发及有效共生真菌的分离和鉴定. 植物生态学报, 36, 859-869.]
[33]	Stewart SL, Kane ME ( 2007). Symbiotic seed germination and evidence for in vitro mycobiont specificity in Spiranthes brevilabris(Orchidaceae) and its implications for species-‍level conservation. In Vitro Cellular & Developmental Biology-Plant, 43, 178-186.
[34]	Stimart DP, Ascher PD ( 1981). In vitro germination of Paphiopedilum seed on a completely defined medium. Scientia Horticulturae, 14, 165-170.
[35]	Swarts ND, Dixon KW ( 2009). Terrestrial orchid conservation in the age of extinction. Annals of Botany, 104, 543-556.
[36]	Vujanovic V, St-Arnaud M, Barabe D, Thibeault G ( 2000). Viability testing of orchid seed and the promotion of colouration and germination. Annals of Botany, 86, 79-86.
[37]	Whitehead MR, Peakall R ( 2014). Pollinator specificity drives strong pre-pollination reproductive isolation in sympatric sexually deceptive orchids. Evolution, 68, 1561-1575.
[38]	Yamazaki J, Miyoshi K ( 2006). In vitro asymbiotic germination of immature seed and formation of protocorm by Cephalanthera falcata(Orchidaceae). Annals of Botany, 98, 1197-1206.
[39]	Zelmer CD, Cuthbertson L, Currah RS ( 1996). Fungi associated with terrestrial orchid mycorrhizas, seeds and protocorms. Mycoscience, 37, 439-448.
[40]	Zettler LW, Piskin KA, Stewart SL, Hartsock JJ, Bowles ML, Bell TJ ( 2005). Protocorm mycobionts of the federally threatened eastern prairie fringed orchid,Platanthera leucophaea(Nutt.) Lindley, and a technique to prompt leaf elongation in seedlings. Studies in Mycology, 53, 163-171.
[41]	Zhou X, Gao JY ( 2016). Highly compatible Epa-01 strain promotes seed germination and protocorm development of Papilionanthe teres(Orchidaceae). Plant Cell Tissue and Organ Culture, 125, 479-493.
[42]	Zi XM, Sheng CL, Goodale UM, Shao SC, Gao JY ( 2014). In situ seed baiting to isolate germination-enhancing fungi for an epiphytic orchid, Dendrobium aphyllum(Orchidaceae). Mycorrhiza, 24, 487-499.
[43]	Zotz G ( 2013). The systematic distribution of vascular epiphytes—A critical update. Botanical Journal of the Linnean Society, 171, 453-481.

多重比较 Multiple comparisons	铁皮石斛 D. officinale			齿瓣石斛 D. devonianum			杂交种 Hybrid
	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate
OMA-MS	-0.139 3 ± 0.058 2^*	0.000 0 ± 0.042 7	0.000 0 ± 0.053 4	-0.044 4 ± 0.071 1	-0.065 5 ± 0.063 9	-0.021 4 ± 0.051 6	-0.012 0 ± 0.058 1	-0.039 3 ± 0.053 0	-0.017 2 ± 0.064 4
OMA-SSCDO-5	-0.235 3 ± 0.057 7^***	-0.888 8 ± 0.042 3^***	-0.696 6 ± 0.052 9^***	0.312 1 ± 0.069 5^***	-0.354 8 ± 0.062 4^***	-0.096 8 ± 0.050 4	-0.036 9 ± 0.058 1	-0.704 0 ± 0.053 0^***	-0.221 3 ± 0.064 4^**
OMA-FDd1	-0.242 3 ± 0.058 2^***	-0.065 5 ± 0.042 7	0.065 5 ± 0.053 4	-0.094 8 ± 0.070 5	-0.651 7 ± 0.063 3^***	-0.436 8 ± 0.051 2^***	-0.070 1 ± 0.059 1	-0.800 4 ± 0.053 9^***	-0.295 3 ± 0.065 5^***
MS-SSCDO-5	-0.096 0 ± 0.058 2	-0.888 8 ± 0.042 7^***	-0.696 6 ± 0.053 4^***	0.356 5 ± 0.068 1^***	-0.289 4 ± 0.061 1^***	-0.075 3 ± 0.049 4	-0.024 9 ± 0.055 3	-0.664 8 ± 0.050 4^***	-0.204 0 ± 0.061 3^**
MS- FDd1	-0.102 9 ± 0.058 7	-0.006 6 ± 0.043 1	0.065 5 ± 0.053 8	-0.050 4 ± 0.069 2	-0.586 2 ± 0.062 1^***	-0.415 4 ± 0.050 2^***	-0.058 1 ± 0.056 3	-0.761 1 ± 0.0513 4^***	-0.278 0 ± 0.062 4^***
SSCDO-5- FDd1	-0.007 0 ± 0.058 2	0.823 3 ± 0.042 7^***	0.631 0 ± 0.053 4^***	-0.406 9 ± 0.067 5^***	-0.296 9 ± 0.060 6^***	-0.340 0 ± 0.049 0^***	-0.033 2 ± 0.056 3	-0.096 4 ± 0.051 3	-0.074 0 ± 0.062 4

多重比较 Multiple comparisons	铁皮石斛 D. officinale			齿瓣石斛 D. devonianum			杂交种 Hybrid
	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate	种子萌发率 Seed germination rate	原球茎形成率 Protocorms formation rate	幼苗率 Seedlings formation rate
OMA-MS	-0.139 3 ± 0.058 2^*	0.000 0 ± 0.042 7	0.000 0 ± 0.053 4	-0.044 4 ± 0.071 1	-0.065 5 ± 0.063 9	-0.021 4 ± 0.051 6	-0.012 0 ± 0.058 1	-0.039 3 ± 0.053 0	-0.017 2 ± 0.064 4
OMA-SSCDO-5	-0.235 3 ± 0.057 7^***	-0.888 8 ± 0.042 3^***	-0.696 6 ± 0.052 9^***	0.312 1 ± 0.069 5^***	-0.354 8 ± 0.062 4^***	-0.096 8 ± 0.050 4	-0.036 9 ± 0.058 1	-0.704 0 ± 0.053 0^***	-0.221 3 ± 0.064 4^**
OMA-FDd1	-0.242 3 ± 0.058 2^***	-0.065 5 ± 0.042 7	0.065 5 ± 0.053 4	-0.094 8 ± 0.070 5	-0.651 7 ± 0.063 3^***	-0.436 8 ± 0.051 2^***	-0.070 1 ± 0.059 1	-0.800 4 ± 0.053 9^***	-0.295 3 ± 0.065 5^***
MS-SSCDO-5	-0.096 0 ± 0.058 2	-0.888 8 ± 0.042 7^***	-0.696 6 ± 0.053 4^***	0.356 5 ± 0.068 1^***	-0.289 4 ± 0.061 1^***	-0.075 3 ± 0.049 4	-0.024 9 ± 0.055 3	-0.664 8 ± 0.050 4^***	-0.204 0 ± 0.061 3^**
MS- FDd1	-0.102 9 ± 0.058 7	-0.006 6 ± 0.043 1	0.065 5 ± 0.053 8	-0.050 4 ± 0.069 2	-0.586 2 ± 0.062 1^***	-0.415 4 ± 0.050 2^***	-0.058 1 ± 0.056 3	-0.761 1 ± 0.0513 4^***	-0.278 0 ± 0.062 4^***
SSCDO-5- FDd1	-0.007 0 ± 0.058 2	0.823 3 ± 0.042 7^***	0.631 0 ± 0.053 4^***	-0.406 9 ± 0.067 5^***	-0.296 9 ± 0.060 6^***	-0.340 0 ± 0.049 0^***	-0.033 2 ± 0.056 3	-0.096 4 ± 0.051 3	-0.074 0 ± 0.062 4