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The Effect of Virulence and Resistance Mechanisms on The International Journal of Molecular Sciences Review The Effect of Virulence and Resistance Mechanisms on the Interactions between Parasitic Plants and Their Hosts Luyang Hu 1, Jiansu Wang 1, Chong Yang 2, Faisal Islam 1, Harro J. Bouwmeester 3 , Stéphane Muños 4 and Weijun Zhou 1,* 1 Institute of Crop Science and Zhejiang Key Lab of Crop Germplasm, Zhejiang University, Hangzhou 310058, China; [email protected] (L.H.); [email protected] (J.W.); [email protected] (F.I.) 2 Bioengineering Research Laboratory, Institute of Bioengineering, Guangdong Academy of Sciences, Guangzhou 510316, China; [email protected] 3 Swammerdam Institute for Life Sciences, University of Amsterdam, 1000 BE Amsterdam, The Netherlands; [email protected] 4 LIPM, Université de Toulouse, INRAE, CNRS, 31326 Castanet-Tolosan, France; [email protected] * Correspondence: [email protected]; Tel.: +86-571-88982770 Received: 31 August 2020; Accepted: 31 October 2020; Published: 27 November 2020 Abstract: Parasitic plants have a unique heterotrophic lifestyle based on the extraction of water and nutrients from host plants. Some parasitic plant species, particularly those of the family Orobanchaceae, attack crops and cause substantial yield losses. The breeding of resistant crop varieties is an inexpensive way to control parasitic weeds, but often does not provide a long-lasting solution because the parasites rapidly evolve to overcome resistance. Understanding mechanisms underlying naturally occurring parasitic plant resistance is of great interest and could help to develop methods to control parasitic plants. In this review, we describe the virulence mechanisms of parasitic plants and resistance mechanisms in their hosts, focusing on obligate root parasites of the genera Orobanche and Striga. We noticed that the resistance (R) genes in the host genome often encode proteins with nucleotide-binding and leucine-rich repeat domains (NLR proteins), hence we proposed a mechanism by which host plants use NLR proteins to activate downstream resistance gene expression. We speculated how parasitic plants and their hosts co-evolved and discussed what drives the evolution of virulence effectors in parasitic plants by considering concepts from similar studies of plant–microbe interaction. Most previous studies have focused on the host rather than the parasite, so we also provided an updated summary of genomic resources for parasitic plants and parasitic genes for further research to test our hypotheses. Finally, we discussed new approaches such as CRISPR/Cas9-mediated genome editing and RNAi silencing that can provide deeper insight into the intriguing life cycle of parasitic plants and could potentially contribute to the development of novel strategies for controlling parasitic weeds, thereby enhancing crop productivity and food security globally. Keywords: parasitic plant; host; virulence; race; resistance mechanism; pathogen effector; evolution; NLR; Orobanche; Striga; interaction model 1. Introduction Parasitic plants have a unique heterotrophic lifestyle in which they obtain water and nutrients from their hosts via an invasive root-like organ known as haustorium [1]. Parasitic plants occur in all terrestrial plant communities and ~4500 species have been described, distributed over 28 families, representing 1% of all dicotyledonous angiosperm species [2]. These parasites have independently Int. J. Mol. Sci. 2020, 21, 9013; doi:10.3390/ijms21239013 www.mdpi.com/journal/ijms Int. J. Mol. Sci. 2020, 21, x FOR PEER REVIEW 2 of 27 1. Introduction Parasitic plants have a unique heterotrophic lifestyle in which they obtain water and nutrients Int. J. Mol. Sci. 2020, 21, 9013 2 of 27 from their hosts via an invasive root-like organ known as haustorium [1]. Parasitic plants occur in all terrestrial plant communities and ~4500 species have been described, distributed over 28 families, representing 1% of all dicotyledonous angiosperm species [2]. These parasites have independently evolved at least 12 or 13 times [3] and unprecedented horizontal gene transfer (HGT) [4] has contributed evolved at least 12 or 13 times [3] and unprecedented horizontal gene transfer (HGT) [4] has to their taxonomic and morphological diversity [1]. Some parasitic plant species attack crops and contributed to their taxonomic and morphological diversity [1]. Some parasitic plant species attack causecrops severe and damage cause andsevere yield damage losses, and particularly yield losses, in particularly the Mediterranean, in the Mediterranean, central and easterncentral and Europe, Africa,eastern and Asia Europe, [5,6 ].Africa, Most and research Asia [5,6]. has focused Most research on the has genera focusedOrobanche, on the genera Striga, Orobanche, Cuscuta, and Striga,Viscum (FigureCuscuta,1). and Viscum (Figure 1). FigureFigure 1. Some 1. Some representative representative parasitic parasitic plantplant species. (a)( aTriphysaria) Triphysaria versicolor versicolor, a hemiparasite,, a hemiparasite, a a photosyntheticallyphotosynthetically competent competent species that, that, facultat facultatively,ively, parasitizes parasitizes rootsroots of neighboring of neighboring plants; ( plants;b) (b) OrobancheOrobanche cumana cumana,, holoparasite, holoparasite, withwith absolute absolute nutritional nutritional dependence dependence on ona host, a host, mainly mainly parasitizes parasitizes rootsroots of sunflower; of sunflower; (c) Cuscuta(c) Cuscuta pentagona pentagona,, holoparasite, holoparasite, also also known known as as dodder, dodder, that that parasitizes parasitizes abovegroundaboveground tissues tissues of both of both monocot monocot and and dicot dicot hosts; hosts; ((d) Striga gesnerioides gesnerioides, an, an obligate obligate hemiparasite hemiparasite that mainlythat mainly parasitizes parasitizes roots roots of cowpea.of cowpea. StrigaStrigaand Orobancheand Orobanchespecies species are are especially especially di difficultfficult to control control in in the the field field due due to their to their large large seedseed banks and special parasitism traits [6], as well as the economic limitations in developing countries, banks and special parasitism traits [6], as well as the economic limitations in developing countries, where these parasites are most prevalent [3]. The life cycles of Striga and Orobanche species are similar where these parasites are most prevalent [3]. The life cycles of Striga and Orobanche species are because they coordinate with the life cycle of the host. The essential steps are germination, radicle similargrowth because to the they host coordinate root, haustorium with the formation life cycle and of attachment the host. to The the essential host root, steps establishment are germination, of a radiclexylem–xylem growth to the connection, host root, and haustorium the production formation of seeds and [7,8]. attachment The host–parasite to the host interaction root, establishment begins with of a xylem–xylemthe secretion connection, of chemical and signals the productionby the host roots of seeds that[ induce7,8]. The the host–parasite germination of interaction parasite seeds begins and with the secretionare called of germination chemical signals stimulants by the [9]. host Accordingly, roots that inducethe inhibition the germination of parasite seed of parasite germination seeds is and a are calledprimary germination target stimulantsfor parasitic [ 9weed]. Accordingly, control [10]. theAlmost inhibition all germination of parasite stimulants seed germination discovered isthus a primary far targetbelong for parasitic to the carotenoid-derived weed control [10]. strigolactone Almost all germination(SL) family [11]. stimulants Recent studies discovered have shown thus far that belong the to the carotenoid-derivedbreeding of crops showing strigolactone limited (SL) exudation family of [11 SLs]. fr Recentom the studies root is an have effective shown strategy that the to breedingachieve of resistance to Orobanche and Striga [12–14]. We, therefore, discussed low SL levels as a natural crops showing limited exudation of SLs from the root is an effective strategy to achieve resistance to Orobanche and Striga [12–14]. We, therefore, discussed low SL levels as a natural resistance mechanism in host plants as well as biotechnological strategies to induce this trait. Other practical methods to control parasitic plants have been extensively reviewed but are often unsuccessful in the long term because the parasite evolves faster than the resistant host, leading to the emergence of distinct races or pathotypes with renewed virulence [6,10,15–18]. The existence of host-specific races suggests that parasites have evolved complex mechanisms to overcome potential host resistance, but most reviews overlook this aspect and focus on the host’s Int. J. Mol. Sci. 2020, 21, 9013 3 of 27 resistance mechanisms. Here, we considered recent examples of virulence and race evolution in parasitic plants before looking at host resistance mechanisms in the context of canonical resistance genes (R genes) encoding proteins with nucleotide-binding and leucine-rich repeat (LRR) domains, often termed “NLR proteins”. We used these to develop a plausible model explaining the molecular basis of host–parasite interactions. We also summarized current genomic resources for parasitic plants and discussed the functions of known virulence genes and their roles in the evolution of host-specific races of parasitic plants. 2. Virulence Evolution in the Family Orobanchaceae 2.1. Definition of Race in
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