Abstract
Taxus, a genus of conifers known for its medicinal significance, faces various conservation challenges with several species classified under different threat categories by the IUCN. The overharvesting of bark and leaves for the well-known chemotherapy drug paclitaxel has resulted in its population decline. Exploring the mycorrhizal relationship in Taxus is of utmost importance, as mycorrhizal fungi play pivotal roles in nutrition, growth, and ecological resilience. Taxus predominantly associates with arbuscular mycorrhizal fungi (AM), and reports suggest ectomycorrhizal (EM) or dual mycorrhizal associations as well. This review consolidates existing literature on mycorrhizal associations in Taxus species, focusing on structural, physiological, and molecular aspects. AM associations are well-documented in Taxus, influencing plant physiology and propagation. Conversely, EM associations remain relatively understudied, with limited evidence suggesting their occurrence. The review highlights the importance of further research to elucidate dual mycorrhizal associations in Taxus, emphasizing the need for detailed structural and physiological examinations to understand their impact on growth and survival.
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Notes
* Taxus species in the Western Himalayas were previously identified as T. baccata, T. wallichiana, or T. fuana but are now recognized as T. contorta.
In 1887, Frank introduced the term “endotrophic mycorrhiza” to describe the mutually beneficial relationships between certain fungi and plant roots lacking a mantle, initially focusing on mycorrhizal associations in Ericaceae and Orchidaceae. Subsequently, another type of endotrophic mycorrhiza formed by non-septate fungi, was identified and termed “phycomycetous mycorrhiza”. This was later replaced by the term “vesicular-arbuscular mycorrhiza,” due to production of vesicles and arbuscules by endotrophic fungi in root cells which was in use for some time. However, the recognition that not all fungi in this symbiosis formed vesicles prompted the proposal to rename it as arbuscular mycorrhiza, a change that has gained widespread acceptance. It is now understood that arbuscular mycorrhiza (AM), ericoid mycorrhiza, and orchid mycorrhiza represent distinct types of “endomycorrhizal” associations, each with unique anatomical features and involving separate host and fungus lineages. Hence, the term “endomycorrhiza” is deemed inappropriate as it encompasses various association types that are phylogenetically and functionally disparate (Brundrett 2004).
References
Adhikari P, Pandey A (2018) Diversity of endophytic fungi associated with himalayan yew (Taxus Wallichiana Zucc.) Roots. Proc Himal Researchers Consortium 1(1):1–9
Albornoz FE, Lambers H, Turner BL, Teste FP, Laliberté E (2016) Shifts in symbiotic associations in plants capable of forming multiple root symbioses across a long-term soil chronosequence. Ecol Evol 6(8):2368–2377. https://doi.org/10.1002/ece3.2000
Anthony MA, Crowther TW, Van Der Linde S, Suz LM, Bidartondo MI, Cox F et al (2022) Forest tree growth is linked to mycorrhizal fungal composition and function across Europe. ISME J 16(5):1327–1336. https://doi.org/10.1038/s41396-021-01159-7
Bakshi BK, Thapar HS (1960) Mycorrhizae in Taxus baccata and Pinus wallichiana. Indian for 86(1):16–17
Boullard B, Ferchau HA (1962) Endotrophic mycorrhizae of plants collected in some eastern American and Canadian white pine communities. Phyton 19(1):65–71
Brundrett M (1991) Mycorrhizas in natural ecosystems. In Advances in ecological research Academic Press, pp 171–313. https://doi.org/10.1016/S0065-2504(08)60099-9
Brundrett M (2004) Diversity and classification of mycorrhizal associations. Biol Rev 79:473–495. https://doi.org/10.1017/S1464793103006316
Brundrett MC, Tedersoo L (2020) Resolving the mycorrhizal status of important northern hemisphere trees. Plant Soil 454:3–34. https://doi.org/10.1007/s11104-020-04627-9
Chaudhuri H (1945) Mycorrhiza of forest trees. Proc 32nd Indian Sci Congr 3(66):548
Chaurasia B, Pandey A, Palni LMS (2004) Occurrence of arbuscular mycorrhizae in the rhizosphere of Himalayan Yew (Taxus baccata L. subsp. wallichiana (Zucc.) Pilger) – A Case Study. In: GK Podila and AK Varma (Eds) Basic research and applications of Mycorrhizae, IK International Pvt. Ltd. New Delhi, pp 26–35
Chen M, Arato M, Borghi L, Nouri E, Reinhardt D (2018) Beneficial services of arbuscular mycorrhizal fungi–from ecology to application. Front Plant Sci 9:1270. https://doi.org/10.3389/fpls.2018.01270
Correa A, Strasser RJ, Martins-Loucao MA (2006) Are Mycorrhiza Always Beneficial? Plant Soil 279: 65–73. https://doi.org/10.1007/s11104-005-7460-1
Coughlan P, Carolan JC, Hook IL, Kilmartin L, Hodkinson TR (2020) Phylogenetics of Taxus using the internal transcribed spacers of nuclear ribosomal DNA and plastid trnL-F regions. Horticulturae 6(1):19. https://doi.org/10.3390/horticulturae6010019
Davison J, Moora M, Öpik M, Adholeya A, Ainsaar L, Bâ A et al (2015) Global assessment of arbuscular mycorrhizal fungus diversity reveals very low endemism. Science 349(6251):970–973. https://doi.org/10.1126/science.aab1161
Ejaz Ahmed EA, Yamin Bibi YB, Muhammad Arshad MA, Kaleem Ullah KU (2014) Conservation status of Taxus floridana, a critically endangered evergreen coniferous plant. Pure Appl Bio 3(4):188–191
Falkowski G, Matysiak B (2010) The use of arbuscular mycorrhizal fungi in container production of selected ornamental conifers under organic-mineral fertilization level. J Fruit Ornam Plant Res 18(2):335–348
Farr K (2008), November Genus-level approach to Taxus species. In Int. Expert Workshop on CITES Non-Detriment Findings, Cancun, Mexico pp. 1–21
Fu X, Zhang G, Wu W, Zhang P, Ren J (2017) Diversity of arbuscular mycorrhizal fungi in rhizosphere soil of Taxus chinensis var. Mairei from different areas. Mycosystema 36(8):1061–1071
Gemma JN, Koske RE, Roberts EM, Hester S (1998) Response of Taxus x media var. Densiformis to inoculation with arbuscular mycorrhizal fungi. Can J for Res 28(1):150–153. https://doi.org/10.1139/x97-182
Griffiths RP, Chadwick AC, Robatzek M, Schauer K, Schaffroth KA (1995) Association of ectomycorrhizal mats with Pacific yew and other understory trees in coniferous forests. Plant soil 173:343–347. https://doi.org/10.1007/BF00011473
Heklau H, Schindler N, Buscot F, Eisenhauer N, Ferlian O, Prada Salcedo LD, Bruelheide H (2021) Mixing tree species associated with arbuscular or ectotrophic mycorrhizae reveals dual mycorrhization and interactive effects on the fungal partners. Ecol Evol 11(10):5424–5440. https://doi.org/10.1002/ece3.7437
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT et al (2010) A meta-analysis of context‐dependency in plant response to inoculation with mycorrhizal fungi. Ecol Let 13(3):394–407. https://doi.org/10.1111/j.1461-0248.2009.01430.x
Iglesias MI, Sainz MJ, Vilariño A, López Mosquera ME, Pintos C, Mansilla JP (2004) Mineral nutrition of Taxus baccata l. as affected by inoculation with arbuscular mycorrhizal fungi. Acta Hortic 630:225–229. https://doi.org/10.17660/ActaHortic.2004.630.28
Kaul K (2008) Variation in rooting behavior of stem cuttings in relation to their origin in Taxus Wallichiana Zucc. New for 36(3):217–224. https://doi.org/10.1007/s11056-008-9094-7
Lambers H, Raven J, Shaver G, Smith S (2008) Plant nutrient-acquisition strategies change with soil age. Trends Ecol Evol 23:95–103. https://doi.org/10.1016/j.tree.2007.10.008
Lee JE, Eom AH (2022) Diversity and community structure of ectomycorrhizal mycorrhizal fungi in roots and rhizosphere soil of Abies Koreana and Taxus cuspidata. Mt Halla Mycobiology 50(6):448–456. https://doi.org/10.1080/12298093.2022.2161974
Li J, Davis CC, Del Tredici P, Donoghue MJ (2001) Phylogeny and biogeography of Taxus (Taxaceae) inferred from sequences of the internal transcribed spacer region of nuclear ribosomal DNA. Harv Pap Bot 6(1):267–274
Liu WC, Gong T, Zhu P (2016) Advances in exploring alternative Taxol sources. RSC Adv 6(54):48800–48809. https://doi.org/10.1039/C6RA06640B
Mai DS, Viet TD, Au VT, Sandor H, Peter S (2012) Studies on the symbiosis between some natural truffles and Taxus Wallichiana Zucc. In Lam Dong Province. Vietnam APCBEE Procedia 4:110–114. https://doi.org/10.1016/j.apcbee.2012.11.019
Mazur S, Nadziakiewicz M, Kurzawińska H, Nawrocki J (2019) Effectiveness of mycorrhizal fungi in the protection of juniper, rose, yew and highbush blueberry against Alternaria alternata. Folia Hortic 31(1):117–127. https://doi.org/10.2478/fhort-2019-0008
Misra A, Srivastava NK, Srivastava AK, Chattopadhyay SK (2010) Influence of gibberellic acid and arbuscular mycorrhizae inoculation on carbon metabolism, growth, and diterpene accumulation in Taxus Wallichiana Zuccarini var. Mairei. J Biophy Struct Biol 2(2):022–027
Mohammadi K, Khalesro S, Sohrabi Y, Heidari G (2011) A review: beneficial effects of the mycorrhizal fungi for plant growth. J Appl Environ Biol Sci 1(9):310–319
Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. In: M, Allen (eds) Mycorrhizal functioning: an integrative plant–fungal process. Chapman and Hall, New York, NY, USA, pp 357–423
Neuenkamp L, Prober SM, Price JN, Zobel M, Standish RJ (2019) Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. Fungal Ecol 40:140–149. https://doi.org/10.1016/j.funeco.2018.05.004
Pandey A, Adhikari P, Dhyani A, Palni LMS (2020) Use of root microbiome in conservation of Himalayan Yew (Taxus Wallichiana Zucc.): an eco-friendly Approach. Natl Acad Sci Lett 44:249–251. https://doi.org/10.1007/s40009-020-00988-y
Pant S, Samant SS (2008) Population ecology of the endangered Himalayan Yew in Khokhan Wildlife Sanctuary of North Western Himalaya for conservation management. J Mt Sci 5:257–264. https://doi.org/10.1007/s11629-008-0078-z
Peterson RL, Massicotte HB (2004) Exploring structural definitions of mycorrhizas, with emphasis on nutrient-exchange interfaces. Canad J Bot 82(8):1074–1088. https://doi.org/10.1139/b04-071
Policelli N, Horton TR, Hudon AT, Patterson TR, Bhatnagar JM (2020) Back to roots: the role of ectomycorrhizal fungi in boreal and temperate forest restoration. Front Glob Change 3:97. https://doi.org/10.3389/ffgc.2020.00097
Poudel RC, Gao LM, Möller M, Baral SR, Uprety Y, Liu J, Li DZ (2013) Yews (Taxus) along the Hindu Kush-Himalayan region: exploring the ethnopharmacological relevance among communities of Mongol and caucasian origins. J Ethnopharmacol 147(1):190–203. https://doi.org/10.1016/j.jep.2013.02.031
Ray P, Ishiga T, Decker SR, Turner GB, Craven KD (2015) A novel delivery system for the root symbiotic fungus, Sebacina Vermifera, and consequent biomass enhancement of low lignin COMT switchgrass lines. Bioenergy Res 8:922–933. https://doi.org/10.1007/s12155-015-9636-8
Redecker D, Schüßler A (2014) Glomeromycota. Systematics and evolution: part a Berlin. Springer, Heidelberg, pp 251–269
Ren JH, Zhang JF, Liu RX, Li YQ (2008) Study on arbuscular mycorrhizae in Taxus chinensis var. Mairei. Acta Bot Bor Occi Sin 28(7):1468–1473
Sainz MJ, Iglesias I, Pintos C, Mansilla JP, Vilarino A (2000) Improved production of nursery stock of Taxus baccata L. through management of the arbuscular mycorrhizal symbiosis. Acta Hortic 536:379–384. https://doi.org/10.17660/ActaHortic.2000.536.45
Scagel CF, Reddy K, Armstrong JM (2003) Mycorrhizal Fungi in rooting substrate influences the quantity and quality of roots on stem cuttings of Hick’s Yew. Horttechnology 13(1):62–66. https://doi.org/10.21273/HORTTECH.13.1.0062
Sharma A, Sagar A, Joshi M (2017) Diversity of fungi associated with Taxus baccata Linn. In different seasons. Indian for 143(4):380–384. https://doi.org/10.36808/if/2017/v143i4/113695
Sharma P (2003) Studies on mycorrhiza and mycorrhizosphere of Taxus baccata Linn. Ph.D. Thesis. Himachal Pradesh University, Shimla
Sáinz MJ, Iglesias I, Vilariño A, Soto J, Pintos C, Mansilla JP (1998) Deacetilbaccatin iii production in mycorrhizal and nonmycorrhizal Taxus baccata l. plants infected with Phytophthora Cinnamomi rands.: preliminary results. Acta Hortic 513:91–98. https://doi.org/10.17660/ActaHortic.1998.513.9
Smith SE, Read DJ (2010) Mycorrhizal symbiosis. Academic
Sohn HY, Okos MR (1998) Paclitaxel (taxol): from nutt to drug. J Microbiol Biotechn 8(5):427–440
Solaiman ZM, Mickan B (2014) Use of mycorrhiza in sustainable agriculture and land restoration. In: Solaiman Z, Abbott L, Varma A (eds) Mycorrhizal Fungi: use in sustainable agriculture and land restoration. Soil Biology, vol 41. Springer, Berlin, Heidelberg, pp 1–15. https://doi.org/10.1007/978-3-662-45370-4_11-15. https://doi.org/10.1007/978-3-662-45370-4_1
Spjut RW (1999) Overview of the Genus Taxus (Taxaceae): the species, their classification, and female reproductive morphology. The World Botanical Associates, Inc Bakersfield, California, p 29
Spjut RW (2007) Taxonomy and nomenclature of Taxus (Taxaceae). J Bot Res Inst Tex 1:203–289
Strullu DG, Gourret JP, Garrec JP, Fourcy A (1981) Ultrastructure and electron-probe microanalysis of the metachromatic vacuolar granules occurring in Taxus mycorrhizas. New Phytol 87(3):537–545. https://doi.org/10.1111/j.1469-8137.1981.tb03224.x
Svenning JC, Magard E (1999) Population ecology and conservation status of the last natural population of English yew Taxus baccata in Denmark. Biol Conserv 88(2):173–182. https://doi.org/10.1016/S0006-3207(98)00106-2
Tapwal A, Kapoor KS, Thakur Y (2022) Growth enhancement in containerized Pinus gerardiana seedlings inoculated with ectomycorrhizal fungi. Arch Microbiol 204(12):724. https://doi.org/10.1007/s00203-022-03328-4
Tedersoo L, Bahram M, Zobel M (2020) How mycorrhizal associations drive plant population and community biology. Science 367(6480):1223. https://doi.org/10.1126/science.aba122
Tedersoo L, Brundrett MC (2017) Evolution of ectomycorrhizal symbiosis in plants. In: L, Tedersoo (eds) Biogeography of mycorrhizal symbiosis. Springer International, Cham, Switzerland, pp 407–467. https://doi.org/10.1007/978-3-319-56363-3
Tedersoo L, Smith ME (2013) Lineages of ectomycorrhizal fungi revisited: foraging strategies and novel lineages revealed by sequences from belowground. Fungal boil Rev 27(3–4):83–99. https://doi.org/10.1016/j.fbr.2013.09.001
Tedersoo L, Sánchez-Ramírez S, Koljalg U, Bahram M, Döring M, Schigel D, May T, Ryberg M, Abarenkov K (2018) High-level classification of the Fungi and a tool for evolutionary ecological analyses. Fungal Divers 90:135–159. https://doi.org/10.1007/s13225-018-0401-0
Teste FP, Jones MD, Dickie IA (2020) Dual-mycorrhizal plants: their ecology and relevance. New Phytol 225(5):1835–1851. https://doi.org/10.1111/nph.16190
Thakur A, Kanwal KS (2024) Assessing the global distribution and conservation status of the Taxus Genus: an overview. Trees People 15:100501. https://doi.org/10.1016/j.tfp.2024.100501
Thoen E, Harder CB, Kauserud H, Botnen SS, Vik U, Taylor AFS, Menkis A, Skrede I (2020) In vitro evidence of root colonization suggests ecological versatility in the genus Mycena. New Phytol 227:601–612. https://doi.org/10.1111/nph.16545
van Der Heijden MG, Martin FM, Selosse MA, Sanders IR (2015) Mycorrhizal ecology and evolution: the past, the present, and the future. New Phytol 205(4):1406–1423. https://doi.org/10.1111/nph.13288
Wang XQ, Ran JH (2014) Evolution and biogeography of gymnosperms. Mol Phylogenetics Evol 75:24–40. https://doi.org/10.1016/j.ympev.2014.02.005
Wani MC, Taylor HL, Wall ME, Coggon P, McPhail AT (1971) Plant Antitumor agents, VI. The isolation and structure oftaxol, a novel antileukemic and antitumor agent from Taxus brevifolia. J Am Chem Soc 93:2325–2327
Wen Y, Uchiyama K, Ueno S, Han W, Xie W, Tsumura Y (2018) Assessment of the genetic diversity and population structure of Maire yew (Taxus chinensis var. Mairei) for conservation purposes. Can J Res 48(5):589–598. https://doi.org/10.1139/cjfr-2017-0429
Wubet T, Weiss M, Kottke I, Oberwinkler F (2003) Morphology and molecular diversity of arbuscular mycorrhizal fungi in wild and cultivated yew (Taxus baccata). Can J Bot 81:255–226. https://doi.org/10.1139/b03-020
Yang Y, Ferguson DK, Liu B, Mao KS, Gao LM, Zhang SZ, Wan T, Rushforth K, Zhang ZX (2022) Recent advances on phylogenomics of gymnosperms and a new classification. Plant Divers 44(4):340–350. https://doi.org/10.1016/j.pld.2022.05.003
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Sharma, N., Tapwal, A. Mycorrhizal symbiosis in Taxus: a review. Mycorrhiza (2024). https://doi.org/10.1007/s00572-024-01148-6
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DOI: https://doi.org/10.1007/s00572-024-01148-6