半寄生植物与寄主间的寄生关系

The parasitic relationship between hemiparasitic plants and host plants

摘要

寄生植物中，半寄生植物约占 80%，它们通过吸器与寄主植物的茎或根部相连，从而与寄主建立寄生关系。尽管体内含有叶绿素，并具备一定的光合能力，半寄生植物仍需从寄主中摄取大量水分和养分以维持生长。半寄生植物长期对寄主进行养分胁迫，不仅严重抑制寄主的生长发育，还会增加其应对环境变化的压力，对农林业带来严重的经济损失。本文系统阐述半寄生植物与寄主间的寄生关系，涵盖吸器形成、结构与功能、寄主偏好性及对寄主的生理影响，并分析其在变化环境下的生存策略，以及半寄生植物在生态系统中的应用与防治方法；同时探讨半寄生植物的研究趋势，对未来研究方向提出展望，包括聚焦吸器发育的动态过程、拓展寄主研究范围、解析环境变化下寄生关系的动态，并整合分子调控手段与抗寄生性状筛选，助力抗寄生物种育种进程，以期为半寄生植物的生理生态特性深入研究提供有益参考。

Abstract

Hemiparasitic plants account for approximately 80% of parasitic species. Although they possess chlorophyll and retain a certain capacity for photosynthesis, these plants establish parasitic connections with their host plants via specialized structures called haustoria, which are attached to the host's stems or roots. Through these connections, hemiparasites extract substantial amounts of water and nutrients from their hosts to sustain their own growth. By imposing long-term nutrient stress on their hosts, hemiparasites not only severely inhibit host growth and development but also exacerbate the host's vulnerability to environmental changes, leading to significant economic losses in agriculture and forestry. A review was made to systematically elaborate on the parasitic relationship between hemiparasitic plants and their hosts, covering the formation, structure, and function of haustoria, host preferences, and the physiological impacts on hosts. This review also analyzes the survival strategies of hemiparasitic plants under changing environments, as well as their applications and control methods in ecosystems. Furthermore, the review discusses research trends in hemiparasitism and proposes future research directions, including focusing on the dynamic processes of haustorial development, expanding the scope of host studies, and elucidating the dynamics of parasitic relationships under environmental changes. Additionally, it highlights the integration of molecular regulation approaches and the screening of anti-parasitic traits to facilitate the breeding of parasitic-resistant species, aiming to provide valuable references for in-depth research into the physiological and ecological characteristics of hemiparasitic plants.

关键词

半寄生植物 / 吸器 / 寄生关系 / 生存策略

Key words

Hemiparasitic plants / haustorium / parasitic relationship / survival strategy

参考文献

[1] Yoshida S, Cui S K, Ichihashi Y, et al. The haustorium, a specialized invasive organ in parasitic plants[J]. Annual Review of Plant Biology, 2016, 67(1): 643-667. https://doi.org/10.1146/annurev-arplant-043015-111702

[2] 李倩. 中国寄生被子植物的多样性、分布及生态[D]. 南京: 南京师范大学, 2019. https://doi.org/10.27245/d.cnki.gnjsu.2019.001052

[3] Nickrent D L. Parasitic angiosperms: how often and how many?[J]. Taxon, 2020, 69(1): 5-27. https://doi.org/10.1002/tax.12195

[4] Scalon M C, Heilmeier H, Rossatto D R. Plant-plant parasitism: trends in the last 50 years and a call for papers for a special issue in Flora[J]. Flora, 2024, 310: 152438. https://doi.org/10.1016/j.flora.2023.152438

[5] Savov S, Marinova B, Teofanova D, et al. Parasitic plants: potential vectors of phytopathogens[J]. Pathogens, 2024, 13(6): 484. https://doi.org/10.3390/pathogens13060484

[6] Hegenauer V, Körner M, Albert M. Plants under stress by parasitic plants[J]. Current Opinion in Plant Biology, 2017, 38: 34-41. https://doi.org/10.1016/j.pbi.2017.04.006

[7] Hartley S E, Green J P, Massey F P, et al. Hemiparasitic plant impacts animal and plant communities across four trophic levels[J]. Ecology, 2015, 96(9): 2408-2416. https://doi.org/10.1890/14-1244.1

[8] Teixeira-Costa L, Davis C C. Life history, diversity, and distribution in parasitic flowering plants[J]. Plant Physiology, 2021, 187(1): 32-51. https://doi.org/10.1093/plphys/kiab279

[9] Kirschner G K, Xiao T T, Jamil M, et al. A roadmap of haustorium morphogenesis in parasitic plants[J]. Journal of Experimental Botany, 2023, 74(22): 7034-7044. https://doi.org/10.1093/jxb/erad284

[10] 周峰, 陈君, 徐荣, 等. 根寄生植物种子萌发刺激物研究进展[J]. 植物生态学报, 2009, 33(3): 607-616. https://doi.org/10.3773/j.issn.1005-264x.2009.03.020

[11] 黄新亚, 管开云, 李爱荣. 寄生植物的生物学特性及生态学效应[J]. 生态学杂志, 2011, 30(8): 1838-1844. https://doi.org/10.13292/j.1000-4890.2011.0278

[12] Bouwmeester H, Li C S, Thiombiano B, et al. Adaptation of the parasitic plant lifecycle: germination is controlled by essential host signaling molecules[J]. Plant Physiology, 2021, 185(4): 1292-1308. https://doi.org/10.1093/plphys/kiaa066

[13] Nelson D C. The mechanism of host-induced germination in root parasitic plants[J]. Plant Physiology, 2021, 185(4): 1353-1873. https://doi.org/10.1093/plphys/kiab043

[14] CHANG M, LYNN D G. The haustorium and the chemistry of host recognition in parasitic angiosperms[J]. Journal of Chemical Ecology, 1986, 12(2): 561-579. https://doi.org/10.1007/bf01020572

[15] Cui S K, Wada S, Tobimatsu Y, et al. Host lignin composition affects haustorium induction in the parasitic plants Phtheirospermum japonicum and Striga hermonthica [J]. New Phytologist, 2018, 218(3): 710-723. https://doi.org/10.1111/nph.15033

[16] Cui S K, Takeda-Kimura Y, Wakatake T, et al. Striga hermonthica induces lignin deposition at the root tip to facilitate prehaustorium formation and obligate parasitism [J]. Plant Communications, 2025, 6(5): 101294. https://doi.org/10.1016/j.xplc.2025.101294

[17] Jhu M Y, Farhi M, Wang L, et al. Heinz-resistant tomato cultivars exhibit a lignin-based resistance to field dodder (Cuscuta campestris) parasitism [J]. Plant Physiology, 2022, 189(1): 129-151. https://doi.org/10.1093/plphys/kiac024

[18] Li L L, Su L, Zhao R X, et al. Sunflower HaWRKY29 dampens Orobanche cumana parasitism via transcriptional activation of HaLAC17 and lignin deposition [J]. Plant Physiology, 2026, 200(3): kiag038. https://doi.org/10.1093/plphys/kiag038

[19] Xiang L, Cui S K, Saucet S B, et al. Glucosylation of endogenous haustorium-inducing factors underpins kin avoidance in parasitic plants[J]. Science, 2025, 390(6771): 405-410. https://doi.org/10.1126/science.adx8220

[20] 卞展, 刘小金, 洪舟, 等. 檀香小 G 蛋白 Rac1 基因的克隆与功能分析[J]. 西北植物学报, 2021, 41(1): 46-51. https://doi.org/10.7606/j.issn.1000-4025.2021.01.0046

[21] Meng S, Bian Z, Wang S K, et al. SaRac1, a small GT-Pase, plays an essential role in haustorium development in the root parasite sandalwood (Santalum album) [J]. Tree Physiology, 2025, 45(12): tpaf147. https://doi.org/10.1093/treephys/tpaf147

[22] Aoki N. Cui S K. Yoshida S. Cytokinins induce prehaustoria coordinately with quinone signals in the parasitic plant Striga hermonthica [J]. Plant and Cell Physiology, 2022, 63(10): 1446-1456. https://doi.org/10.1093/pcp/pcac130

[23] ISHIDA J K, WAKATAKE T, YOSHIDA S, et al. Local auxin biosynthesis mediated by a YUCCA Flavin monooxygenase regulates haustorium development in the parasitic plant Phtheirospermum japonicum [J]. The Plant Cell, 2016, 28(8): 1795-1814. https://doi.org/10.1105/tpc.16.00310

[24] Tomilov A A, Tomilova N B, Abdallah I, et al. Localized hormone fluxes and early haustorium development in the hemiparasitic plant Triphysaria versicolor [J]. Plant Physiology, 2005, 138(3): 1469-1480. https://doi.org/10.1104/pp.104.057836

[25] Pan L M, Wan L Y, Song L S, et al. Comparative proteomic analysis provides new insights into the development of haustorium in Taxillus chinensis (DC.) danser [J]. BioMed Research International, 2022, 2022: 9567647. https://doi.org/10.1155/2022/9567647

[26] Gurney A L, Grimanelli D, Kanampiu F, et al. Novel sources of resistance to Striga hermonthica in Tripsacum dactyloides, a wild relative of maize [J]. New Phytologist, 2003, 160(3): 557-568. https://doi.org/10.1046/j.1469-8137.2003.00904.x

[27] Pielach A, Leroux O, Domozych D S, et al. Arabinogalactan protein-rich cell walls, paramural deposits and ergastic globules define the hyaline bodies of rhinanthoid Orobanchaceae haustoria[J]. Annals of Botany, 2014, 114(6): 1359-1373. https://doi.org/10.1093/aob/mcu121

[28] Irving L J, Cameron D D. You are what you eat: interactions between root parasitic plants and their hosts[J]. Advances in Botanical Research, 2009, 50: 87-138.

[29] Makaza W, En-Nahli Y, Amri M. Harnessing plant resistance against Striga spp. parasitism in major cereal crops for enhanced crop production and food security in Sub-Saharan Africa: a review [J]. Food Security, 2023, 15(5): 1127-1149. https://doi.org/10.1007/s12571-023-01345-9

[30] Huang X Y, Zhang Y B, Scalon M C, et al. Survival secrets of mistletoes: high drought tolerance in canopy habitats[J]. Tree Physiology, 2025, 45(7): tpaf071. https://doi.org/10.1093/treephys/tpaf071

[31] Press M C, Graves J D, Stewart G R. Transpiration and carbon acquisition in root hemiparasitic angiosperms[J]. Journal of Experimental Botany, 1988, 39(8): 1009-1014. https://doi.org/10.1093/jxb/39.8.1009

[32] Kim G, Westwood J H. Macromolecule exchange in Cuscuta-host plant interactions[J]. Current Opinion in Plant Biology, 2015, 26: 20-25. https://doi.org/10.1016/j.pbi.2015.05.012

[33] Smith J D, Mescher M C, De Moraes C M. Implications of bioactive solute transfer from hosts to parasitic plants[J]. Current Opinion in Plant Biology, 2013, 16(4): 464-472. https://doi.org/10.1016/j.pbi.2013.06.033

[34] Péron T, Candat A, Montiel G, et al. New insights into phloem unloading and expression of sucrose transporters in vegetative sinks of the parasitic plant Phelipanche ramosa L. (Pomel) [J]. Frontiers in Plant Science, 2017, 7: 2048. https://doi.org/10.3389/fpls.2016.02048

[35] Jiang F, Veselova S, Veselov D, et al. Cytokinin flows from hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite cytokinins relations [J]. Functional Plant Biology, 2005, 32(7): 619-629. https://doi.org/10.1071/fp04168

[36] Lu J K, Kang L H, Sprent J I, et al. Two-way transfer of nitrogen between Dalbergia odorifera and its hemiparasite Santalum album is enhanced when the host is effectively nodulated and fixing nitrogen [J]. Tree Physiology, 2013, 33(5): 464-474. https://doi.org/10.1093/treephys/tpt024

[37] Yoshida S, Maruyama S, Nozaki H, et al. Horizontal gene transfer by the parasitic plant Striga hermonthica [J]. Science, 2010, 328(5982): 1128. https://doi.org/10.1126/science.1187145

[38] Zhang D L, Qi J F, Yue J P, et al. Root parasitic plant Orobanche aegyptiaca and shoot parasitic plant Cuscuta australis obtained Brassicaceae-specific strictosidine synthase-like genes by horizontal gene transfer [J]. BMC Plant Biology, 2014, 14: 19. https://doi.org/10.1186/1471-2229-14-19

[39] Calvin C L, Wilson C A. Epiparasitism in Phoradendron durangense and P. falcatum (Viscaceae) [J]. Aliso, 2009, 27(1): 2. https://doi.org/10.5642/Aliso.20092701.02

[40] 蒋若衍. 中国寄生被子植物的分布及其与寄主的关系[D]. 南京: 南京师范大学, 2021.

[41] Bowie M, Ward D. Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality [J]. Journal of Arid Environments, 2004, 56(3): 487-508. https://doi.org/10.1016/S0140-1963(03)00067-3

[42] Ehleringer J R, Schulze E D, Ziegler H, et al. Xylem-tapping mistletoes: water or nutrient parasites?[J]. Science, 1985, 227(4693): 1479-1481. https://doi.org/10.1126/science.227.4693.1479

[43] Schulze E D, Ehleringer J R. The effect of nitrogen supply on growth and water-use efficiency of xylem-tapping mistletoes[J]. Planta, 1984, 162(3): 268-275. https://doi.org/10.1007/bf00397449

[44] Seel W E, Cooper R E, Press M C. Growth, gas exchange and water use efficiency of the facultative hemiparasite Rhinanthus minor associated with hosts differing in foliar nitrogen concentration [J]. Physiologia Plantarum, 1993, 89(1): 64-70. https://doi.org/10.1111/j.1399-3054.1993.tb01787.x

[45] Kim C W, An C H, Lee H S, et al. Proximate and mineral components of Viscum album var. coloratum grown on eight different host tree species [J]. Journal of Forestry Research, 2019, 30(4): 1245-1253. https://doi.org/10.1007/s11676-018-0730-6

[46] Adler L S, Karban R, Strauss S Y. Direct and indirect effects of alkaloids on plant fitness via herbivory and pollination[J]. Ecology, 2001, 82: 2032-2044. https://doi.org/10.1890/0012-9658

[47] Barhoumi Z, Atia A, Hussain A A, et al. Host-hemiparasite Acacia gerrardii - Phragmanthera austroarabica relationship: physiological and biochemical aspects [J]. Phytoparasitica, 2025, 53(4): 79. https://doi.org/10.1007/s12600-025-01300-8

[48] Press M C, Phoenix G K. Impacts of parasitic plants on natural communities[J]. New Phytologist, 2005, 166(3): 737-751. https://doi.org/10.1111/j.1469-8137.2005.01358.x

[49] Cameron D D, Coats A M, Seel W E. Differential resistance among host and non-host species underlies the variable success of the hemi-parasitic plant Rhinanthus minor [J]. Annals of Botany, 2006, 98(6): 1289-1299. https://doi.org/10.1093/aob/mcl218

[50] Dörr I. How Striga parasitizes its host: a TEM and SEM study[J]. Annals of Botany, 1997, 79(5): 463-472. https://doi.org/10.1006/anbo.1996.0385

[51] Cirocco R M, Facelli J M, Watling J R. Does nitrogen affect the interaction between a native hemiparasite and its native or introduced leguminous hosts?[J]. New Phytologist, 2017, 213(2): 812-821. https://doi.org/10.1111/nph.14181

[52] 高发明. 云杉矮槲寄生的发生特征分析及其对青杄光合与蒸腾作用的影响[D]. 北京: 北京林业大学, 2014.

[53] Govier R N, Nelson M D, Pate J S. Hemiparasitic nutrition in angiosperms[J]. New Phytologist, 1967, 66(2): 285-297. https://doi.org/10.1111/j.1469-8137.1967.tb06006.x

[54] Těšitel J, Plavcová L, Cameron D D. Interactions between hemiparasitic plants and their hosts[J]. Plant Signaling & Behavior, 2010, 5(9): 1072-1076. https://doi.org/10.4161/psb.5.9.12563

[55] Rigling A, Eilmann B, Koechli R, et al. Mistletoe-induced crown degradation in Scots pine in a xeric environment[J]. Tree Physiology, 2010, 30(7): 845-852. https://doi.org/10.1093/treephys/tpq038

[56] Scalon M C, Wright I J. Leaf trait adaptations of xylem-tapping mistletoes and their hosts in sites of contrasting aridity[J]. Plant and Soil, 2017, 415(1): 117-130. https://doi.org/10.1007/s11104-016-3151-3

[57] Zhang Y B, Corrêa Scalon M, Liu J X, et al. You are what you eat: nutrient and water relations between mistletoes and hosts[J]. New Phytologist, 2023, 238(2): 567-583. https://doi.org/10.1111/nph.18747

[58] Radomiljac A M, Mccomb J A, Pate J S. Gas exchange and water relations of the root hemi-parasite Santalum album L. in association with legume and non-legume hosts[J]. Annals of Botany, 1999, 83(3): 215-224. https://doi.org/10.1006/anbo.1998.0815

[59] Barhoumi Z. Physiological and biochemical attributes of the association host-parasite (Tamarix aphylla- Plicosepalus acacia) [J]. Plant Physiology and Biochemistry, 2024, 216: 109163. https://doi.org/10.1016/j.plaphy.2024.109163

[60] Těšitel J, Li A R, Knotková K, et al. The bright side of parasitic plants: what are they good for? [J]. Plant Physiology, 2021, 185(4): 1309-1324. https://doi.org/10.1093/plphys/kiaa069

[61] Heide-Jørgensen H S. Parasitic flowering plants [M]. Boston: Brill, 2008: 1-438. https://doi.org/10.1163/ej.9789004167506.i-438

[62] WATLING J R, PRESS M C. Impacts of Infection by Parasitic Angiosperms on Host Photosynthesis [J]. Plant Biology, 2001, 3: 244-50. https://doi.org/10.1055/s-2001-15195

[63] Koenig W D, Knops J M H, Carmen W J, et al. Effects of mistletoe (Phoradendron villosum) on California oaks [J]. Biology Letters, 2018, 14(6): 20180240. https://doi.org/10.1098/rsbl.2018.0240

[64] Yan C F, Gessler A, Rigling A, et al. Effects of mistletoe removal on growth, N and C reserves, and carbon and oxygen isotope composition in Scots pine hosts[J]. Tree Physiology, 2016, 36(5): 562-575. https://doi.org/10.1093/treephys/tpw024

[65] Zhang Y B, Huang X Y, Corrêa Scalon M, et al. Mistletoes have higher hydraulic safety but lower efficiency in xylem traits than their hosts[J]. New Phytologist, 2025, 245(2): 607-624. https://doi.org/10.1111/nph.20257

[66] Jiang F, Jeschke W D, Hartung W. Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations [J]. Journal of Experimental Botany, 2004, 55(406): 2323-2329. https://doi.org/10.1093/jxb/erh240

[67] Světlíková P, Hájek T, Těšitel J. Water-stress physiology of Rhinanthus alectorolophus, a root-hemiparasitic plant [J]. PLoS One, 2018, 13(8): e0200927. https://doi.org/10.1371/journal.pone.0200927

[68] Reid N, Yan Z G, Fittler J. Impact of mistletoes (Amyema miquelii) on host (Eucalyptus blakelyi and Eucalyptus melliodora) survival and growth in temperate Australia [J]. Forest Ecology and Management, 1994, 70(1/3): 55-65. https://doi.org/10.1016/0378-1127(94)90074-4

[69] Watson D M, Mclellan R C, Fontúrbel F E. Functional roles of parasitic plants in a warming world[J]. Annual Review of Ecology, Evolution, and Systematics, 2022, 53(1): 25-45. https://doi.org/10.1146/annurev-ecolsys-102320-115331

[70] Hettenhausen C, Li J, Zhuang H, et al. Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants [J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(32): E6703-E6709. https://doi.org/10.1073/pnas.1704536114

[71] Song J, Bian J G, Xue N, et al. Inter-species mRNA transfer among green peach aphids, dodder parasites, and cucumber host plants[J]. Plant Diversity, 2022, 44(1): 1-10. https://doi.org/10.1016/j.pld.2021.03.004

[72] Li Z S, Wang S K, Meng S, et al. Haustorium connection between parasitic Santalum album (sandalwood) and herbivore-damaged Dalbergia odorifera mediates the associational effect to an enhanced herbivory resistance in neighboring sandalwood [J]. Industrial Crops and Products, 2025, 229: 121046. https://doi.org/10.1016/j.indcrop.2025.121046

[73] Těšitel J, Mládek J, Horník J, et al. Suppressing competitive dominants and community restoration with native parasitic plants using the hemiparasitic Rhinanthus alectorolophus and the dominant grass Calamagrostis epigejos [J]. Journal of Applied Ecology, 2017, 54(5): 1487-1495. https://doi.org/10.1111/1365-2664.12889

[74] Knotková K, Těšitelová T, Knotek A, et al. Biocontrol by a native hemiparasite: rapid suppression of noxious invasive plants in a field experiment[J]. Journal of Applied Ecology, 2025, 62(12): 3514-3524. https://doi.org/10.1111/1365-2664.70183

[75] Gobena D, Shimels M, Rich P J, et al. Mutation in sorghum low germination stimulant 1 alters strigolactones and causes Striga resistance [J]. Proceedings of the National Academy of Sciences of the United States of America, 2017, 114(17): 4471-4476. https://doi.org/10.1073/pnas.1618965114

[76] Shi J Y, Mei C, Ge F Y, et al. Resistance to Striga parasitism through reduction of strigolactone exudation [J]. Cell, 2025, 188(7): 1955-1966. e13. https://doi.org/10.1016/j.cell.2025.01.022

[77] Bao G S, Song M L, Wang Y Q, et al. Does Epichloë endophyte enhance host tolerance to root hemiparasite?[J]. Microbial Ecology, 2021, 82(1): 35-48. https://doi.org/10.1007/s00248-020-01496-8

[78] Li A R, Guan K Y, Stonor R, et al. Direct and indirect influences of arbuscular mycorrhizal fungi on phosphorus uptake by two root hemiparasitic Pedicularis species: do the fungal partners matter at low colonization levels?[J]. Annals of Botany, 2013, 112(6): 1089-1098. https://doi.org/10.1093/aob/mct177

[79] Sui X L, Zhang T, Tian Y Q, et al. A neglected alliance in battles against parasitic plants: arbuscular mycorrhizal and rhizobial symbioses alleviate damage to a legume host by root hemiparasitic Pedicularis species [J]. New Phytologist, 2019, 221(1): 470-481. https://doi.org/10.1111/nph.15379

基金资助

中国林科院中央级公益性科研院所基本科研业务费专项资金项目(CAFYBB2024QG006)

广东省林业科技创新项目(2022KJCX023)