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Molecular Dialog Between Parasitic Plants and Their Hosts

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Molecular Dialog Between Parasitic Plants and Their Hosts PY57CH13_Westwood ARjats.cls July 31, 2019 11:22 Annual Review of Phytopathology Molecular Dialog Between Parasitic Plants and Their Hosts Christopher R. Clarke,1 Michael P. Timko,2 John I. Yoder,3 Michael J. Axtell,4 and James H. Westwood5 1Genetic Improvement for Fruits and Vegetables Laboratory, Beltsville Agricultural Research Center, United States Department of Agriculture, Agricultural Research Service, Beltsville, Maryland 20705, USA 2Department of Biology, University of Virginia, Charlottesville, Virginia 22904, USA 3Department of Plant Sciences, University of California, Davis, California 95616, USA 4Department of Biology and Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, Pennsylvania 16802, USA 5School of Plant and Environmental Sciences, Virginia Tech,Blacksburg, Virginia 24061, USA; email: [email protected] Annu. Rev. Phytopathol. 2019. 57:279–99 Keywords First published as a Review in Advance on parasitic plants, Orobanche, Striga, Cuscuta, RNA exchange, haustorium June 21, 2019 The Annual Review of Phytopathology is online at Abstract phyto.annualreviews.org Parasitic plants steal sugars, water, and other nutrients from host plants https://doi.org/10.1146/annurev-phyto-082718- through a haustorial connection. Several species of parasitic plants such as 100043 witchweeds (Striga spp.) and broomrapes (Orobanche and Phelipanche spp.) Annu. Rev. Phytopathol. 2019.57:279-299. Downloaded from www.annualreviews.org Copyright © 2019 by Annual Reviews. are major biotic constraints to agricultural production. Parasitic plants are All rights reserved understudied compared with other major classes of plant pathogens, but Access provided by 2001:468:c80:8104:5ddd:c954:f24e:41ad on 05/29/20. For personal use only. the recent availability of genomic and transcriptomic data has accelerated the rate of discovery of the molecular mechanisms underpinning plant parasitism. Here, we review the current body of knowledge of how parasitic plants sense host plants, germinate, form parasitic haustorial connections, and suppress host plant immune responses. Additionally, we assess whether parasitic plants ft within the current paradigms used to understand the molecular mechanisms of microbial plant–pathogen interactions. Finally, we discuss challenges facing parasitic plant research and propose the most urgent questions that need to be answered to advance our understanding of plant parasitism. 279 PY57CH13_Westwood ARjats.cls July 31, 2019 11:22 INTRODUCTION Parasitic plants live by obtaining part or all of their nutritional needs from another plant. The evo- Parasitic plant: plant lution of parasitism as a life strategy in angiosperms represents the transition of species from au- that receives all or part totrophy to an association with—and, in many cases, obligate dependence on—other plant species. of its nutrients This dependence is associated with parasitic plants evolving mechanisms that enable them to iden- through a haustorial tify host plants, grow invasively into the hosts, and establish connections to withdraw water and connection to another plant resources from the hosts. As such, parasitic plants illustrate some of the most exciting examples of plant–plant interactions. Host plant: plant that Parasitism as a life strategy is widespread among living species, and plants are no exception provides resources to parasitic plants, likely (99). Indeed, the ability to form parasitic associations has evolved independently at least 12 times at a ftness cost in different plant families (136), and parasitic plants account for roughly 1% of angiosperm species. Parasitism, therefore, can demonstrably provide a ftness beneft to plants in multiple ecological Hemiparasite: parasitic plant that can contexts. One trait common among parasites is the need to obtain water and mineral nutrients photosynthesize and from their hosts, suggesting that access to water and nitrogen is a driving factor in this evolution thus is not completely (52). In terms of dependency on host photosynthesis and metabolism, large differences exist among dependent on the host parasitic plant species, spanning the spectrum from hemiparasite to holoparasite and facultative plant for sugars to obligate parasites. Nevertheless, it is important to note that all parasitic plants evolved from Holoparasite: autotrophic ancestors, so at the cellular level, they retain the distinctive features of plants such as parasitic plant that plastids and cell walls. lacks the capacity for At the whole-plant level, parasitic plants exhibit a wide range of different morphologies and photosynthesis and thus relies entirely on structurally different haustorial connections. The haustorium connects parasites to their hosts and uptake of sugars from provides a conduit for extracting host resources. As a result, parasite species are freed from many host plants of the normal constraints of autotrophic plants; they may also have reduced or absent organs such Facultative parasite: as roots or leaves and may lack chlorophyll. Some species exist primarily underground, attached to a parasitic plant that host roots, emerging above the soil only to fower (e.g., Phelipanche and Orobanche). Other species can complete its may pass substantial portions of their vegetative life cycle growing inside their hosts (e.g., Raffesia, lifecycle as an mistletoes). For the latter, the shelter provided by living underground or within the host could autotrophic plant but provide another advantage for parasitism. But given the diverse origins of parasitic plants, it is retains the capacity to opportunistically diffcult to generalize among the various types. parasitize host plants. The Orobanchaceae and Cuscutaceae families have received the most research attention to date Facultative parasitic (Figure 1) because they include some of the most economically important parasitic weed species. plants must be Orobanchaceae are root parasites and include the genera Striga (witchweed) and Alectra,which hemiparasitic pose a great threat to cereal production in sub-Saharan Africa, India, and Asia (94). The related Haustorium: organ species in Phelipanche and Orobanche (together commonly called broomrapes) destroy yields of that invades the host broad-leaved crops throughout North Africa, the Mediterranean, Europe, and the Middle East. and forms a physical Annu. Rev. Phytopathol. 2019.57:279-299. Downloaded from www.annualreviews.org Although the hemiparasites Triphysaria versicolor and Phtheirospermum japonicum are not weedy, and physiological bridge between they have been developed into model parasite species that can be readily cultured in the laboratory Access provided by 2001:468:c80:8104:5ddd:c954:f24e:41ad on 05/29/20. For personal use only. parasite and host and genetically transformed (54, 121). Besides the Orobanchaceae, Cuscuta species are important stem parasites that cause substantial economic impact (94) and have increasingly become the sub- ject of parasitic plant research. All these species have contributed to exciting developments in our understanding of the mechanisms of parasite–host interactions. The study of parasitic plants spans the disciplines of weed science and plant pathology. On the one hand, these parasites are angiosperms and have the same basic biochemistry, genetics, and physiology as do fully autotrophic plants. From an agronomic perspective, parasitic weeds may be controlled in part by mechanical or chemical methods similar to those used on autotrophic weeds, thus falling under the purview of weed science (4, 30, 37). On the other hand, parasitic plants may deviate substantially from fully autotrophic plants in terms of physiology and morphology because they behave like pathogens, with specifc adaptations for acquiring resources from their 280 Clarke et al. PY57CH13_Westwood ARjats.cls July 31, 2019 11:22 Phelipanche Orobanche Striga Triphysaria Phtheirospermum Cuscuta aegyptiaca crenata hermonthica versicolor japonicum campestris a c e g i k Parasite b d f Parasite h jl Host root Parasite Parasite Host root Host root Parasite Host root Host root Obligate parasites Facultative parasites Obligate Orobanchaceae Cuscutaceae Figure 1 Some of the most widely studied parasitic plant species. The top row shows a typical view of the parasite, and the bottom row shows examples of parasite–host connections. Phelipanche aegyptiaca is shown on (a)tomatoand(b) Arabidopsis, Orobanche crenata on (c)faba bean and (d) lentil root, Striga hermonthica on (e,f ) sorghum, Triphysaria versicolor (g) in the feld and (h) connected to the root of the unknown host. Phtheirospermum japonicum is shown (i) in the feld and ( j) connected to rice root via two haustoria. Cuscuta campestris is shown (k)ontomatoand(l) as a close-up of the haustorial region on beet. Photos provided by (a,b,c,e,k,l) James Westwood, (d)Rashid Mentag, (f ) Michael Timko, (g,h) John Yoder, and (i,j) Satoko Yoshida. hosts. Researchers have described multiple levels of parasitic plant signaling, including the specifc triggering of germination of parasite seeds by host root exudates, tropic growth of the parasite radicle/stem toward the host, and initiation of the haustorium as well as myriad chemical and physical interactions that mediate the haustorial interaction with host tissues (Figure 2). This review focuses on recent advances in parasitic plant biology that relate to these interactions and support the consideration of parasitic plants as plant pathogens. Annu. Rev. Phytopathol. 2019.57:279-299. Downloaded
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