Parasitic plant cultivation: examples, lessons learned and future directions
DOI:
https://doi.org/10.24823/Sibbaldia.2022.1892Keywords:
parasitic plants, cultivation,, propagation, conservation, Rafflesia, botanic gardensAbstract
Parasitic plants contain some of the most bizarre and fascinating organisms in the plant kingdom. Yet they are notable for their absence from botanic gardens’ plant collections and conservation strategies. Besides a handful of species, few are widespread in cultivation; indeed we estimate at least 76 per cent of species are entirely missing from collections today, and most of these have never been grown at all. Here, we place focus on the holoparasites, a group of plants long neglected due to their difficulty in cultivation. We review propagation breakthroughs in temperate and tropical botanic gardens to identify guiding principles for the cultivation of these neglected plants. We document the life cycle of a range of parasitic plants, and assess successful and failed attempts to propagate Rafflesia specifically, which has been the focus of decades of research. By uniting isolated case studies from around the world, we identify future directions for the cultivation and possible ex situ conservation of these botanical enigmas at a time when this is needed urgently. Finally, we recommend a dedicated global community of purpose as an intentional step forward: this could take the form of a Global Consortium for Conservation for parasitic plants, or a Parasitic Plant Specialist Group under the International Union for Conservation of Nature.
References
ABDULLAH, N., HASNIDA HASSAN, N., FUAD YAHYA, M., ABD WAHID, M.S. & AYOP, N. (2020). Preliminary study on establishment of Rafflesia cantleyi in tissue culture using seeds and primordial flower bud as explants. International Journal of Agriculture, Forestry and Plantation, 10: 314–318.
AKIYAMA, K., MATSUZAKI, K.-I. & HAYASHI, H. (2005). Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi. Nature, 435: 824–827.
BAO, Y.Z., YAO, Z.Q., CAO, X.L., PENG, J.F., XU, Y., CHEN, M.X. & ZHAO, S.F. (2017). Transcriptome analysis of Phelipanche aegyptiaca seed germination mechanisms stimulated by fluridone, TIS108, and GR24. PLoS One, 12: e0187539. doi: https://doi.org/10.1371/journal.pone.0187539
BARKER, E.R., PRESS, M.C., SCHOLES, J.D. & QUICK, W.P. (1996). Interactions between the parasitic angiosperm Orobanche aegyptiaca and its tomato host: growth and biomass allocation. New Phytologist, 133: 637–642. doi: https://doi.org/10.1111/j.1469-8137.1996.tb01932.x
BASKIN, C.C. & BASKIN, J.M. (2014). Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination (2nd edn). Academic Press, San Diego, CA.
BASKIN, C.C. & BASKIN, J.M. (2021). Germination and seed/embryo size in holoparasitic flowering plants with ‘dust seeds’ and an undifferentiated embryo. The Botanical Review. doi: https://doi.org/10.1007/s12229-020-09242-y
BECK, G. (1890). Monographie der Gattung Orobanche. Bibliotheca Botanica 19. Cassel.
BOEWIG, H. (1904). The histology and development of Cassytha filiformis L. Contributions from the Botanical Laboratory of the University of Pennsylvania, 2: 399–416.
BOTANIC GARDENS CONSERVATION INTERNATIONAL (2022a). PlantSearch online database. Available online: https://tools.bgci.org/plant_search.php (accessed January 2022).
BOTANIC GARDENS CONSERVATION INTERNATIONAL (2022b). ThreatSearch online database. Available online: https://tools.bgci.org/threat_search.php (accessed January 2022).
BOUWMEESTER, H., LI, C., THIOMBIANO, B., RAHIMI, M. & LEENG DONG, L. (2021). Adaptation of the parasitic plant lifecycle: germination is controlled by essential host signaling molecules. Plant Physiology, 185: 1292–1308. doi: https://doi.org/10.1093/plphys/kiaa066
CARLQUIST, S. (1989). Hydnora in my garden! Haustorium – Parasitic Plant Newsletter, 21: 2–3.
CARTELLIERI, E. (1928). Das Hautorium von Cassytha pubescens R.Br. Planta, 6(1): 162–182.
CULLEN, J. (2010). 662. Phelypaea boissieri. Orobanchaceae. Curtis’s Botanical Magazine, 26(4): 379–388. doi: https://doi.org/10.1111/j.1467-8748.2009.01673.x
FARAH, A.F. (1987). Some ecological aspects of Cistanche phelypaea (L.) Cout. (Orobanchaceae) in Al-Hasa Oasis, Saudi Arabia. In: WEBER, H.C. & FORSTREUTER, W. (eds), Parasitic Flowering Plants. Proceedings of the 4th ISPFP, Marburg 1987, pp. 187–196.
FAY, M.F., BENNETT, J.R., DIXON, K.W. & CHRISTENHUSZ, M.J.M. (2010). Parasites, their relationships and the disintegration of Scrophulariaceae sensu Lato. Curtis‘s Botanical Magazine, 26(4): 286–313. doi: https://doi.org/10.1111/j.1467-8748.2009.01668.x
FLEISCHMANN, A. (2013). Orobanche elatior in Bayern. Berichte der Bayerischen Botanischen Gesellschaft, 83: 187–191.
FURMAN, T.E. & TRAPPE, J.M. (1971). Phylogeny and ecology of mycotrophic achlorophyllous angiosperms. Quarterly Review of Biology, 46(3): 219–225. doi: https://doi.org/10.1086/406896
HEIDE-JØRGENSEN, H.S. (2008). Parasitic Flowering Plants. Brill, Leiden.
HEINRICHER, E. (1907). Beiträge zur Kenntnis der Gattung Balanophora [Contributions to the knowledge of the genus Balanophora]. Sitzungsberichte der Kaiserlichen Akademie der Wissenschaften in Wien, Mathematisch-naturwissenschaftliche Klasse, 116: 439–465.
HEINRICHER, E. (1910). Die Aufzucht und Kultur der parasitischen Samenpflanzen [The Rearing and Cultivation of Parasitic Seed Plants]. Fischer, Jena.
HEINRICHER, E. (1915). Die Keimung und Entwicklungsgeschichte der Wachholdermistel, Arceuthobium Oxycedri, auf Grund durchgeführter Kulturen geschildert [Germination and ontogeny of the dwarf mistletoe, Arceuthobium oxycedri, based on cultivation experiments]. Sitzungsberichte der Kaiserlichen Akademie zu Wien, 124: 89–90.
HEINRICHER, E. (1917). Die erste Aufzucht einer Rafflesiacee, Cytinus Hypocistis L., aus Samen [First rearing of a Rafflesiaceae, Cytinus hypocistis L., from seed]. Berichte der Deutschen Botanischen Gesellschaft, 35: 505–513.
HEINRICHER, E. (1922). Methoden der Aufzucht und Kultur der parasitischen Samenpflanzen [Methods of rearing and cultivating parasitic flowering plants]. Abderhalden’s Handbuch der biologischen Arbeitsmethoden, vol. 11. Urban & Schwarzenberg, Vienna & Leipzig.
HIBBERD, J.M., QUICK, W.P., PRESS, M.C. & SCHOLES, J.D. (1998). Can source–sink relations explain responses of tobacco to infection by the root holoparasitic angiosperm Orobanche cernua? Plant, Cell & Environment, 21: 333–340. doi: https://doi.org/10.1046/j.1365-3040.1998.00272.x
HIDAYATI, S.N., MEIJER, W., BASKIN, J.M. & WALCK, J.L. (2000). A contribution to the life history of the rare Indonesian holoparasite Rafflesia patma (Rafflesiaceae). Biotropica, 32: 404–414.
JOEL, D.M., GRESSEL, J. & MUSSELMAN, L.J. (EDS) (2013). Parasitic Orobanchaceae. Parasitic Mechanisms and Control Strategies. Springer, Berlin & Heidelberg.
KAHONO, S., MURSIDAWATI, S. & ERNIWATI, E. (2010). Insects community on the flower of Rafflesia patma Blume (Rafflesiaceae) in its non native habitat of Bogor Botanical Gardens, Bogor City, Province of West Java, Indonesia. Jurnal Biologi Indonesia, 6(3): 429–442 [in Indonesian].
KUIJT, J. (1966). Greenhouse culture of two Neotropical mistletoes. Journal of the Royal Horticultural Society, 41(9): 400–402.
KUIJT, J. (1969). The Biology of Parasitic Flowering Plants. University of California Press, Berkeley, CA.
KUIJT, J. (1986). Observations on establishment and early shoot emergence of Viscum minimum (Viscaceae). Botanica Neerlandica, 35(4): 449–456.
LEI, D., THOROGOOD, C.J., TU, P., SONG, Y., HUANG, L., ALDUGHAYMAN, M., LEON, C.J. & HAWKINS, J.A. (2021). Cistanche deserticola: Orobanchaceae. Curtis’s Botanical Magazine, 38(4): 472–486. doi: https://doi.org/10.1111/curt.12413
MATUSOVA, R., MOURIK, T. & BOUWMEESTER, H. (2004). Changes in the sensitivity of parasitic weed seeds to germination stimulants. Seed Science Research, 14(4): 335–344. doi: 10.1079/SSR2004187
MEIJER, W. (1997). Rafflesiaceae. Flora Malesiana Bulletin (ser. 1) 13: 1–42.
MOLINA, J., MCLAUGHLIN, W., WALLICK, K., PEDALES, R., MARIUS, V.M., TANDANG, D.N., DAMATAC, A., STUHR, N., PELL, S.K., LIM, T.M. & NOVY, A. (2017). Ex situ propagation of Philippine Rafflesia in the United States: challenges and prospects. Sibbaldia, 15: 77–96. doi: https://doi.org/10.24823/Sibbaldia.2017.224
MOUNCE, R., SMITH, P. & BROCKINGTON, S. (2017). Ex situ conservation of plant diversity in the world’s botanic gardens. Nature Plants, 3: 795–802. doi: https://doi.org/10.1038/s41477-017-0019-3
MURSIDAWATI, S. (2012). Fruit and seed morphology of Rafflesia patma and R. arnoldii. Buletin Kebun Raya, 15(1): 21–30 [in Indonesian].
MURSIDAWATI, S. (2017). Ex situ conservation of Rafflesia patma (Rafflesiaceae) in Bogor Botanical Gardens (Indonesia). Nature Conservation Research, 2(2): 90–91. doi: https://doi.org/10.24189/ncr.2017.014
MURSIDAWATI, S. & HANDINI, E. (2009). Biologi konservasi tumbuhan holoparasit: percobaan kultur in vitro [Conservation biology of holoparasites: in vitro culture experiments]. Proceedings of Indonesian Flora Conservation in Addressing the Impact of Global Warming, July 14 2009, ‘Eka Karya’ Botanical Garden, Tabanan, Bali, pp. 158–162.
MURSIDAWATI, S. & IRAWATI, I. (2017). Biologi Konservasi Rafflesia. LIPI-Press, Jakarta.
MURSIDAWATI, S., IRAWATI, I. & NGATARI, N. (2014). Rafflesia patma (Rafflesiaceae): notes on its field study, cultivation, seed germination and anatomy. Buletin Kebun Raya, 17(1): 9–14.
MURSIDAWATI, S., NGATARI, N., IRAWATI, I., CARDINAL, S. & KUSUMAWATI, R. (2015). Ex-situ conservation of Rafflesia patma Blume (Rafflesiaceae) – an endangered emblematic parasitic species from Indonesia. Sibbaldia, 13: 99–109. doi: https://doi.org/10.24823/Sibbaldia.2015.77
MURSIDAWATI, S. & SUNARYO, S. (2012). Anatomical study of the endophytic Rafflesia patma inside the host Tetrastigma sp. Buletin Kebun Raya, 15(2): 71–80 [in Indonesian].
MURSIDAWATI, S., WICAKSONO, A. & TEIXEIRA DA SILVA, J.A. (2019). Development of the endophytic parasite, Rafflesia patma Blume, among host plant (Tetrastigma leucostaphylum (Dennst.) Alston) vascular cambium tissue. South African Journal of Botany, 123: 382–386. doi: https://doi.org/10.1016/j.sajb.2019.03.028
MURSIDAWATI, S., WICAKSONO, A. & TEIXEIRA DA SILVA, J.A. (2020). Rafflesia patma Blume flower organs: histology of the epidermis and vascular structures, and a search for stomata. Planta, 251: 112. doi: https://doi.org/10.1007/s00425-020-03402-5
MURSIDAWATI, S. & WICAKSONO, A. (2020). Tissue differentiation of the early and the late flower buds of Rafflesia patma. Journal of Plant Development, 27: 19–32. doi: https://doi.org/10.33628/jpd.2020.27.1.19
MUSSELMAN, L.J. (1977). Seed germination and seedlings of Krameria lanceolata (Krameriaceae). Sida, 7(2): 224–225.
NAIS, J. (2001). Rafflesia of the World. Sabah Parks, Sabah.
NICKRENT, D.L. (2020). Parasitic angiosperms: how often and how many? Taxon, 69: 5–27. doi: https://doi.org/10.1002/tax.12195
NIKOLOV, L.A., ENDRESS, P.K., SUGUMARAN, M., SASIRAT, S., VESSABUTR, S., KRAMER, E.M. & DAVIS, C.C. (2013). Developmental origins of the world’s largest flowers, Rafflesiaceae. Proceedings of the National Academy of Sciences of the United States of America, 110: 18578–18583.
NIKOLOV, L.A. & DAVIS, C.C. (2017). The big, the bad, and the beautiful: biology of the world’s largest flowers. Journal of Systematics and Evolution, 55: 516–524.
NING, M., QUN, G., YU, L. & SHENGGONG, L. (2021). Overview of the measures and techniques used to protect traffic lines against shifting sands in China. Journal of Resources and Ecology, 12(1): 124–135. doi: https://doi.org/10.5814/j.issn.1674-764x.2021.01.012
NORTH, T., CHONG, C., CROSS, A.T., VAN DER WALT, K. & BALLESTEROS, D. (2021). Special collections and under-represented taxa in Australasian ex situ conservation programs. In: MARTYN YENSON, A.J., OFFORD, C.A., MEAGHER, P.F., AULD, T., BUSH, D., COATES, D.J., COMMANDER, L.E., GUJA, L.K., NORTON S.L., MAKINSON, R.O., STANLEY, R., WALSH N. ET AL. (eds), Plant Germplasm Conservation in Australia (3rd edn). Australian Network for Plant Conservation and the Australian Seed Bank Partnership. Available online: www.anpc.asn.au/wp-content/uploads/2021/09/GermplasmGuidelinesThirdEdition_FINAL_210902.pdf (accessed February 2022).
ORLOVSKY, N. & BIRNBAUM, E. (2002). The role of Haloxylon species for combating desertification in Central Asia. Plant Biosystems, 136(2): 233–240. doi: 10.1080/11263500212331351139
PELSER, P.B., NICKRENT, D.L., CALLADO, J.R.C. & BARCELONA, J.F. (2013). Mt. Banahaw reveals: the resurrection and neotypification of the name Rafflesia lagascae (Rafflesiaceae) and clues to the dispersal of Rafflesia seeds. Phytotaxa, 131: 35–40. doi: https://doi.org/10.11646/phytotaxa.131.1.6
POWO (2022). Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. Available online: www.plantsoftheworldonline.org (accessed February 2022).
PRESS, M.C. & GRAVES, J.D. (EDS) (1995). Parasitic Plants. Chapman & Hall, London.
PRESS, M.C. & PHOENIX, G.K. (2005). Impacts of parasitic plants on natural communities. New Phytologist, 166: 737–751. doi: https://doi.org/10.1111/j.1469-8137.2005.01358.x
PUSCH, J. (2009). Orobanche. In: WAGENITZ, G. (ED.), Hegi Illustrierte Flora von Mitteleuropa, Band VI, Teil 1A, Lieferung 1 (3rd edn). Weissdorn-Verlag, Jena.
SEDGLEY, M. (1984). Quandong propagation. Australian Horticulture, 82: 52–59.
SETH, K.J. (2020). Growing paintbrush. International Rock Gardener, 128: 53–60.
SINCLAIR, W.T., MILL, R.R., GARDNER, M.F., WOLTZ, P., JAFFRE, T., PRESTON, J., HOLLINGSWORTH, M.L., PONGE, A. & MOLLER, M. (2002). Evolutionary relationships of the New Caledonian heterotrophic conifer, Parasitaxus usta (Podocarpaceae), inferred from chloroplast trnL-F intron/spacer and nuclear rDNA ITS2 sequences. Plant Systematics and Evolution, 233: 79–104. doi: https://doi.org/10.1007/s00606-002-0199-8
SONG, Y., ZENG, K., JIANG, Y. & TU, P. (2021). Cistanches Herba, from an endangered species to a big brand of Chinese medicine. Medicinal Research Reviews, 41(3): 1539–1577. doi: https://doi.org/10.1002/med.21768
SUKAMTO, L.A. & MUJIONO, M. (2010). In vitro culture of holoparasite Rafflesia arnoldii R. Brown. Buletin Kebun Raya, 13(2): 79–85.
SUSATYA, A. (2007). Taxonomy and ecology of Rafflesia in Bengkulu, Indonesia. Unpublished PhD thesis, University Kebangsaan, Malaysia.
TEIXEIRA-COSTA, L. & DAVIS, C.C. (2021). Life history, diversity, and distribution in parasitic flowering plants. Plant Physiology, 187: 32–51. doi: https://doi.org/10.1093/plphys/kiab279
TERYOKHIN, E.S. (1997). Weed Broomrapes – Systematics, Ontogenesis, Biology, Evolution. Aufstieg-Verlag, Landshut.
THOROGOOD, C.J. (2020). Astonishing plants. Trends in Plant Science, 25(9): 833–836. doi: https://doi.org/10.1016/j.tplants.2020.06.007
THOROGOOD, C.J. (2021). The University of Oxford Botanic Garden: sharing the scientific wonder and importance of plants with the world. Curtis’s Botanical Magazine, 38: 438–450. doi: https://doi.org/10.1111/curt.12419
THOROGOOD, C.J. & HISCOCK, S.J. (2010a). Compatibility interactions at the cellular level provide the basis for host specificity in the parasitic plant Orobanche. New Phytologist, 186: 571–575. doi: https://doi.org/10.1111/j.1469-8137.2009.03173.x
THOROGOOD, C.J. & HISCOCK, S.J. (2010b). Specific developmental pathways underlie host specificity in the parasitic plant Orobanche. Plant Signal and Behavior, 5(3): 275–277. doi: https://doi.org/10.4161/psb.5.3.10660
THOROGOOD, C.J., LEON, C.J., LEI, D., ALDUGHAYMAN, M., HUANG, L.-F. & HAWKINS, J.A. (2021a). Desert hyacinths: an obscure solution to a global problem? Plants, People, Planet, 3: 302–307. doi: https://doi.org/10.1002/ppp3.10215
THOROGOOD, C.J. & RUMSEY, F.J. (2021). Broomrapes of Britain and Ireland. BSBI Handbook No. 22. Botanical Society of Britain and Ireland, Durham.
THOROGOOD, C.J., TEIXEIRA-COSTA, L., CECCANTINI, G., DAVIS, C. & HISCOCK, S.J. (2021b). Endoparasitic plants and fungi show evolutionary convergence across phylogenetic divisions. New Phytologist, 232: 1159–1167. doi: https://doi.org/10.1111/nph.17556
UHLICH, H., PUSCH, J. & BARTHEL, K.J. (1995). Die Sommerwurzarten Europas [Broomrape species of Europe]. Westarp Wissenschaften, Magdeburg.
VIELDKAMP, J.F. (2007). Some notes on the cultivation of Rafflesia. Flora Malesiana Bulletin, 14: 50–53.
WATSON, D.M., MCGREGOR, H.W. & SPOONER, P.G. (2011). Hemiparasitic shrubs increase resource availability and multi-trophic diversity of eucalypt forest birds. Functional Ecology, 25(4): 889–899. doi: https://doi.org/10.1111/j.1365-2435.2011.01839.x
WEBER, H.C. (1981). Untersuchungen an parasitischen Scrophulariaceen (Rhinanthoideen) in Kultur. 1. Keimung und Entwicklungsweise [Studies in cultivated parasitic Scrophulariaceae (Rhinanthoideae). 1. Germination and development]. Flora, 171: 23–38.
WEBER, H.C., FORSTMEIER, L., FORSTREUTER, W., NIETFELD, U. & NIETFELD, U. (1980). Parasitische Blütepflanzen im Garten [Parasitic flowering plants in the garden]. Gartenpraxis, 6: 256–258.
WEIGEND, M. & DOSTERT, N. (2005). Towards a standardization of biological sustainability: wildcrafting Rhatany (Krameria lappacea) in Peru. Medical Plant Conservation, 11: 24–27.
WICAKSONO, A., MURSIDAWATI, S. & MOLINA, J. (2020). A plant within a plant: insights on the development of the Rafflesia endophyte within its host. Botanical Review, 87: 233–242. doi: https://doi.org/10.1007/s12229-020-09236-w
WICAKSONO, A., MURSIDAWATI, S., SUKAMTO, L.A. & TEIXEIRA DA SILVA, J.A. (2016). Rafflesia spp.: propagation and conservation. Planta, 244: 289–296. doi: https://doi.org/10.1007/s00425-016-2512-8
WICAKSONO, A., TEIXEIRA DA SILVA, J.A. & MURSIDAWATI, S. (2017). Dispersal of Rafflesia patma Blume endophyte in grafted host plant (Tetrastigma leucostaphylum (Dennst.) Alston). Journal of Plant Development, 24: 145–150.
XU, R., CHEN, J., CHEN, S.-L., LIU, T.-N., ZHU, W.-C. & XU, J. (2009). Cistanche deserticola Ma cultivated as a new crop in China. Genetic Resources and Crop Evolution, 56: 137–142. doi: https://doi.org/10.1007/s10722-008-9383-1
YAO, Z., TIAN, F., CAO, X., XU, Y., CHEN, M., XIANG, B. & ZHAO, S. (2016). Global transcriptomic analysis reveals the mechanism of Phelipanche aegyptiaca seed germination. International Journal of Molecular Sciences, 17(7): 1139. doi: https://doi.org/10.3390/ijms17071139
YOSHIDA, S. & SHIRASU, K. (2009). Multiple layers of incompatibility to the parasitic witchweed, Striga hermonthica. New Phytologist, 183: 180–189. doi: https://doi.org/10.1111/j.1469-8137.2009.02840.x
ZÁZVORKA, J. (2010). Orobanche kochii and O. elatior (Orobanchaceae) in central Europe. Acta Musei Moraviae, Scientiae biologicae, 95(2): 77–119.
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