Bouwmeester, H.

Scholes, J.

Sinha, N.

English

International Migration, Integration and Social Cohesion online publications

UvA-DARE is a service provided by the library of the University of Amsterdam (https://dare.uva.nl)UvA-DARE (Digital Academic Repository)Parasitic plantsPhysiology, development, signaling, and ecosystem interactionsBouwmeester, H.; Sinha, N.; Scholes, J.DOI10.1093/plphys/kiab055Publication date2021Document VersionFinal published versionPublished inPlant PhysiologyLicenseCC BYLink to publicationCitation for published version (APA):Bouwmeester, H., Sinha, N., & Scholes, J. (2021). Parasitic plants: Physiology, development,signaling, and ecosystem interactions. Plant Physiology, 185(4), 1267-1269.https://doi.org/10.1093/plphys/kiab055General rightsIt is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s)and/or copyright holder(s), other than for strictly personal, individual use, unless the work is under an opencontent license (like Creative Commons).Disclaimer/Complaints regulationsIf you believe that digital publication of certain material infringes any of your rights or (privacy) interests, pleaselet the Library know, stating your reasons. In case of a legitimate complaint, the Library will make the materialinaccessible and/or remove it from the website. Please Ask the Library: https://uba.uva.nl/en/contact, or a letterto: Library of the University of Amsterdam, Secretariat, Singel 425, 1012 WP Amsterdam, The Netherlands. Youwill be contacted as soon as possible.Download date:10 Mar 2023Parasitic plants: physiology, development, signaling,and ecosystem interactionsHarro Bouwmeester ,1,*,† Neelima Sinha2 and Julie Scholes31 Swammerdam Institute for Life Sciences, University of Amsterdam, PO Box 94215, Amsterdam, 1090GE, The Netherlands2 Department of Plant Biology, University of California, Davis, CA 95616, USA3 Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK*Author for communication: H.J.Bouwmeester@uva.nl (H.B.).†Senior author.The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in theInstructions for Authors (https://academic.oup.com/plphys/pages/general-instructions) is: Harro Bouwmeester (H.J.Bouwmeester@uva.nl).Parasitic plants connect to the vasculature of a host plantand take part or all of the water, nutrients, and assimilatesthey need to complete their life cycle. Parasitic plants repre-sent a unique model for the evolution of intra-kingdomparasitism with intriguing research questions such as howplants were able to evolve the ability to parasitize otherplants. This parasitic lifestyle required the evolution of hostdetection, host attachment, host exploitation, and host de-fense suppression strategies. The elucidation of these strate-gies and the underlying mechanisms has been greatlyfacilitated by the advent of model species, molecular and ge-nomic tools, and omics approaches such as transcriptomicsand comparative genomics and this has launched parasiticplant research into the 21st century. The scientific data gen-erated are helping us to gradually unravel how parasitism inplants has evolved. However, parasitic plants are not just aninteresting basic research model. Due to their parasiticlifestyle, many parasitic plant species represent importantagricultural weeds, such as the witchweeds, broomrapes,dodders, and mistletoes. Fundamental knowledge of themechanisms underlying parasitism will also contribute tonew approaches to create resistance in crops and developnew control measures for this important agriculturalproblem.This Focus Issue on Parasitic Plants addresses some of themost important advances and new landmarks in the field. Inaddition to commissioned updates by experts in their re-spective topics, several research articles highlight recentaccomplishments in these areas.The name “parasitic plant” illustrates that these plantsgrow at the expense of their hosts and can cause problemsin agriculture, as will be further discussed below. But para-sitic plants are also an essential component of biodiverseecosystems. In two updates, Casadesús and Munné-Bosch(2021) and Tesitel et al. (2021) describe the role of parasiticplants in natural ecosystems. Casadesús and Munné-Bosch (2021) highlight the role of holoparasitic plant–hostinteractions (such as those between Cytinus hypocistis andvarious shrubs of the genus Cistus) in shaping naturalMediterranean ecosystems. Tesitel et al. (2021) discuss howparasitic plants can also positively influence the growth and/or reproductive output of their host or other, nonhost,organisms and that they can have positive effects on com-munity structure and ecosystem processes. Tesitel et al.(2021) also review the roles that parasitic plants may haveas food or medicinal resources or for aesthetic and culturalpurposes.During the early days of genomics, it was assumed thatparasitic plants must have acquired pathogenicity genesthrough horizontal gene transfer. Surprisingly, in the last de-cade or so it also became clear that pathogenicity evolvedfrom extant physiological processes also present in nonpara-sitic plant species. This Focus Issue contains several exam-ples of the recruitment by parasitic plants of genes involvedin these extant physiological processes, to facilitate aspectsof the parasitic process. A prime example is the coordina-tion of the parasitic plant lifecycle with that of the host,aided by a number of host detection/host response mecha-nisms that have evolved in parasitic plant species. In the up-date by Brun et al. (2021), the molecular mechanismsunderlying two of these—host-dependent seed germinationand haustorium formation—are reviewed. The key processEditorialVC The Author(s) 2021. Published by Oxford University Press on behalf of American Society of Plant Biologists.This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution,and reproduction in any medium, provided the original work is properly cited.Open Accessdoi:10.1093/plphys/kiab055 PLANT PHYSIOLOGY 2021: 185: 1267–1269Downloaded from https://academic.oup.com/plphys/article/185/4/1267/6248938 by guest on 24 April 2022of germination in parasitic plants in response to moleculesexuded by their host is also discussed in the updates byBouwmeester et al. (2021) and Nelson (2021) and in the re-search article by Wang et al. (2021). Especially in theOrobanchaceae, germination in response to chemical hostcues—particularly the strigolactones—is a striking exampleof the evolution of a host detection mechanism. Intriguingly,strigolactones have been shown to be essential hostsignaling molecules, making them reliable cues for theparasites (Bouwmeester et al., 2021). Also, the evolution of aperception mechanism by parasitic plants for the germina-tion stimulants, especially strigolactones, by recruitinghomologs of a receptor KARRIKIN INSENSITIVE 2 (KAI2)/HYPOSENSITIVE TO LIGHT (HTL) and modification of theirligand-binding cavities to allow binding of strigolactones,and their possible role in host selection is highly intriguing(Bouwmeester et al., 2021; Brun et al., 2021; Nelson, 2021).In their research article, Wang et al. (2021) study one ofthese germination stimulant receptors, ShHTL7, in more de-tail and demonstrate the key role of the strigolactone-induced interaction of ShHTL7 with F-Box protein MOREAXILLARY GROWTH 2 (MAX2) and repressor of gene ex-pression, SUPPRESSOR OF MORE AXILLARY GROWTH21 (SMAX1) and the effect of this complex formation on thesensitivity to strigolactones.Just as for regulation of germination, parasitic plants seemto have hijacked extant physiological processes for theattachment to and penetration of host plant tissues bythe haustorium. Haustorium formation is an intriguingprocess, divided into three phases by Brun et al. (2021): (1)attachment to host tissue, (2) penetration of the host, and(3) connection to the host vasculature. The authors reviewthe current knowledge on the role of haustorium inducingfactors (phenolic molecules secreted by the host that inducehaustorium formation), plant hormones such as cytokininand auxin, cell-wall degrading enzymes produced by the par-asite, and avoiding host detection in haustorium formation.In two research articles by Masumoto et al. (2021) andOgawa et al. (2021), new insights into these processes arepresented. Masumoto et al. (2021) report a three-dimensional reconstruction of the haustorium of the obli-gate parasite Striga hermonthica and the facultative parasitePhtheirospermum japonicum. Using this reconstruction incombination with field-emission scanning electron micros-copy they reveal the spatial arrangements of multiple celltypes inside haustoria and their interaction with the hostroot, and highlight differences between the two parasites,particularly with regard to the xylem connection with thehost.Ogawa et al. (2021) investigated differential gene expres-sion in the intrusive cells of P. japonicum and used pro-moter analyses to characterize a number of the differentiallyexpressed genes they identified. They pay particular atten-tion to four subtilisin-like serine proteases, which, uponoverexpression, inhibited both intrusive cell and xylembridge development, suggesting they play an important rolein haustorium development in P. japonicum.The haustorium plays an essential role in the transfer ofassimilates, amino acids, and nutrients from the host to theparasite. In a research article, Zhang et al. (2021) show thatdodder transfers systemic signals, including long-distancemobile mRNAs, with information on the nitrogen status,from one host to another. They demonstrate that these sys-temic signals are able to regulate large transcriptome andDNA methylome changes in the recipient hosts. Intriguingly,in the case of host species soybean and cucumber, signalsproduced by N-starved soybean, induced increased N uptakeactivity in cucumber.Parasitic plants have not only recruited extant physiologi-cal processes, to support their parasitic lifestyle, they havealso lost certain functions. An intriguing example of this isthe loss of photosynthesis, and many of the genes requiredfor that process, by holoparsitic species such as the broom-rapes. Intriguingly, in their research article, Gua et al. (2021)demonstrate that the biosynthesis of phylloquinone, in-volved in photosystem I electron transport and disulfidebridge formation of photosystem II subunits, is retained bythe nonphotosynthetic holoparasite Phelipanche aegyptiaca.The authors suggest that nonphotosynthetic holoparasitesexploit alternative targeting of phylloquinone for transmem-brane redox signaling associated with parasitism.Research on parasitic plants has greatly benefited fromthe ever growing genomics toolkit. To support comparativegenomics work on parasitic plants, Kösters et al. (2021) in aBreakthrough Technologies paper describe a new tool, theWeb Application for the Research of Parasitic Plants(WARPP). WARPP should facilitate international efforts byproviding a central hub of curated evolutionary, ecological,and genetic data on parasitic plants. The tool includes a ge-nome browser for parasitic plant genomes, an orthogroupsummary table, and a tool to explore ancestral traits.WARPP hopes to benefit from contributions from the scien-tific community, see https://parasiticplants.app.The advances in our knowledge underlying the relation-ship between hosts and parasitic plants, have greatly im-proved our understanding of the evolution of plantparasitism. Moreover, it is facilitating the development ofmore effective control measures in cases where these para-sitic plants have developed into agricultural weeds. Thethreat imposed to agriculture by these weeds is nicely illus-trated in the research article by Masanga et al. (2021). Theyreveal the presence of field dodder (Cuscuta campestris) andC. kilimanjari (both either naturalized or endemic to EastAfrica), and for the first time in continental Africa, the pres-ence of the giant dodder (C. reflexa) a south Asian species.These parasites have a wide host range, parasitizing speciesacross 13 angiosperm orders. They studied the potential riskof C. reflexa expanding its host range to important woodycash crops such as tea, coffee, and mango and revealed suc-cessful parasitism, following haustorial formation and vascu-lar bundle connections in all three crops. Modeling furthersupported the threat, by predicting high habitat suitabilityfor all three Cuscuta species across major tea- and coffee-growing regions of Eastern Africa.1268 | PLANT PHYSIOLOGY 2021: 185; 1267–1269 EditorialDownloaded from https://academic.oup.com/plphys/article/185/4/1267/6248938 by guest on 24 April 2022In addition to the large agricultural problems with para-sitic plants in the African continent, the Mediterranean isheavily plagued by broomrape problems in a multitude ofcrops. In their research article, Casadesús and Munné-Bosch (2021) discuss the impact of these broomrapes infect-ing economically important dicotyledonous crops inMediterranean agroecosystems.In an update, Jamil et al. (2021) describe how our growingknowledge of the mechanisms underlying plant parasitismcan be used to improve their control, both through (modern)breeding and through smart agricultural practices and agro-chemistry. In order to be able to introduce resistance intocrops, knowledge of the underlying mechanisms is required.Intriguingly, most hosts are unable to detect an infection byplant parasites or are unable to fend them off. In their up-date, Albert et al. (2021) review examples of hosts that haveevolved defense strategies to avoid infection or protect them-selves actively post-attack often leading to full or partial resis-tance. They discuss the current state of our understanding ofthe defense strategies to plant parasitism used by host plantswith emphasis on the active molecular resistance mechanismsand outline the perspectives and the potential of future stud-ies needed to develop and breed-resistant crops.We hope that the contents of this focus issue will draw at-tention to the importance of parasitic plants in natural andagricultural ecosystems. Using physiological, biochemical,structural, developmental, and genomics tools the authorshave shed light on fundamental processes involved in theparasitism process and the host response to parasitism.ReferencesAlbert M, Axtell MJ, Timko M (2021) Mechanisms of resistance andvirulence in parasitic plant–host interactions. Plant Physiol 185:1282–1291Bouwmeester H, Li C, Thiombiano B, Rahimi M, Dong L (2021)Adaptation of the parasitic plant lifecycle. Germination is con-trolled by essential host signaling molecules. Plant Physiol 185:1292–1308Brun G, Spallek T, Simier P, Delavault P (2021) Molecular actors ofseed germination and haustoriogenesis in parasitic weeds. PlantPhysiol 185: 1270–1281Casadesús A, Munne-Bosch S (2021) Holoparasitic plant-host inter-actions and their impact on Mediterranean ecosystems. PlantPhysiol 185: 1325–1338Gua X, Chen I-G, Harding SA, Nyamdari B, Ortega MA,Clermonte K, Westwood JH, Tsai C-J (2021). Plasma membranephylloquinone biosynthesis in nonphotosynthetic parasitic plants.Plant Physiol 185: 1443–1456Jamil M, Kountche BA, Al-Babili S (2021) Current progress in Strigamanagement. Plant Physiol 185: 1339–1352Kösters LM, Wiechers S, Lyko1 P, Müller KF, Wick S (2021)WARPP 1 - web application for the research of parasitic plants.Plant Physiol 185: 1374–1380Masanga J, Mwangi BN, Kibet W, Sagero P, Wamalwa M, OduorR, Ngugi M, Alakonya A, Ojola P, Bellis E, et al. (2021)Physiological and ecological warnings that Dodder pose an exigentthreat to farmlands in Eastern Africa. Plant Physiol 185: 1457–1467Masumoto N, Suzuki Y, Cui S, Wakazaki M, Sato M, Kumaishi K,Shibata A, Furuta KM, Ichihashi Y, Shirasu K, et al. (2021).Three-dimensional reconstructions of the internal structures of haus-toria in parasitic Orobanchaceae. Plant Physiol 185: 1429–1442Nelson D (2021) The mechanism of host-induced germination inroot parasitic plants. Plant Physiol 185: 1353–1373Ogawa S, Wakatakea T, Spallek T, Ishidaa JK, Sano R, Kurata T,Demura T, Yoshida S, Ichihashi Y, Schaller A, et al. (2021)Subtilase activity in the intrusive cells mediates haustorium matu-ration in parasitic plants. Plant Physiol 185: 1381–1394Tesitel J, Li A-R, Knotkováa K, McLellan R, Bandaranayake PCG,Watson DM (2021) The bright side of parasitic plants: what arethey good for?. Plant Physiol 185: 1309–1324Wang Y, Yao R, Du X, Guo L, Chen L, Xie D, Smith SM (2021)Molecular basis for high ligand sensitivity and selectivity of strigo-lactone receptors in Striga. Plant Physiol 185: 1411–1428Zhang J, Xu Y, Xie J, Zhuang H, Liu H, Shen G, Wu J (2021)Parasite dodder enables transfer of bidirectional systemic nitrogensignals between host plants. Plant Physiol 185: 1395–1410Plant Physiology, 2021, Vol. 185, No. 4 PLANT PHYSIOLOGY 2021: 185; 1267–1269 | 1269Downloaded from https://academic.oup.com/plphys/article/185/4/1267/6248938 by guest on 24 April 2022

Parasitic plants:Physiology, development, signaling, and ecosystem interactions

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Parasitic plants:Physiology, development, signaling, and ecosystem interactions

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