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Management of Infection by Parasitic Weeds: a Review

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Management of Infection by Parasitic Weeds: a Review plants Review Management of Infection by Parasitic Weeds: A Review Mónica Fernández-Aparicio 1,*, Philippe Delavault 2 and Michael P. Timko 3 1 Institute for Sustainable Agriculture, Consejo Superior de Investigaciones Científicas (CSIC), 14004 Córdoba, Spain 2 Laboratory of Plant Biology and Pathology, University of Nantes, 44035 Nantes, France; [email protected] 3 Department of Biology University of Virginia, Charlottesville, VA 22904-4328, USA; [email protected] * Correspondence: [email protected] Received: 27 July 2020; Accepted: 9 September 2020; Published: 11 September 2020 Abstract: Parasitic plants rely on neighboring host plants to complete their life cycle, forming vascular connections through which they withdraw needed nutritive resources. In natural ecosystems, parasitic plants form one component of the plant community and parasitism contributes to overall community balance. In contrast, when parasitic plants become established in low biodiversified agroecosystems, their persistence causes tremendous yield losses rendering agricultural lands uncultivable. The control of parasitic weeds is challenging because there are few sources of crop resistance and it is difficult to apply controlling methods selective enough to kill the weeds without damaging the crop to which they are physically and biochemically attached. The management of parasitic weeds is also hindered by their high fecundity, dispersal efficiency, persistent seedbank, and rapid responses to changes in agricultural practices, which allow them to adapt to new hosts and manifest increased aggressiveness against new resistant cultivars. New understanding of the physiological and molecular mechanisms behind the processes of germination and haustorium development, and behind the crop resistant response, in addition to the discovery of new targets for herbicides and bioherbicides will guide researchers on the design of modern agricultural strategies for more effective, durable, and health compatible parasitic weed control. Keywords: Orobanche; Phelipanche; Striga; Cuscuta; germination; haustorium; crop resistance; bioherbicides; virulence; sustainable control 1. Introduction Approximately 1% of all angiosperms are parasitic on other plants and these plants are distributed among 28 dicotyledonous families having evolved the parasitic lifestyle independently at least 12 times [1–5]. Some are facultative parasites, capable of living autotrophically until reproduction, but shifting to a parasitic life form when a host is available to obtain nutrients with less investment in assimilation system. In comparison, obligated parasitic plants require the infection of another plant to survive shortly after germination. Parasitic plants can be also grouped by their photosynthesis competency, being either photosynthetically active hemiparasites or achlorophyllous holoparasites; or separated based upon the type of vascular connections they form with their host, being either xylem feeders or phloem feeders. They can also be grouped by the host plant organ to which they attach, either root feeders or shoot feeders [4,6]. While many parasitic plants have remained part of larger ecological communities, a small number of species have evolved to weediness, becoming troublesome pests in the agricultural field and an important constraint to crop productivity. Besides colonizing agroecosystems, parasitic plants are also present in urban ecosystems (Figure1). Plants 2020, 9, 1184; doi:10.3390/plants9091184 www.mdpi.com/journal/plants Plants 2020, 9, x FOR PEER REVIEW 2 of 26 productivity.Plants 2020, 9, 1184 Besides colonizing agroecosystems, parasitic plants are also present in urban2 of 26 ecosystems (Figure 1). Figure 1.1.Adaptation Adaptation of parasiticof parasitic plants plants to agricultural to agri andcultural urban and ecosystems. urban ecosystems. Shown are representative Shown are representativephotographs of photographs parasitic plants of para in agriculturalsitic plants in (A ,agriculturalB) and urban (A (,CB,)D and) locations. urban (C (,AD)) Hemiparasiticlocations. (A) Hemiparasiticshoot parasite Viscumshoot parasitesp. feeding Viscum on sp. olive feeding tree; ( Bon) holoparasiticolive tree; (B) root holoparasitic parasite Orobanche root parasitesp. feedingOrobanche on sp.clover feeding commercial on clover field; commercial (C) Viscum field;sp., (C in) Viscum the city sp., of Dijon,in the France;city of Dijon, (D) Orobanche France; (Dsp.) Orobanche parasitizing sp. parasitizingclover in a park clover in thein a city park of in Dijon, the city France. of Dijon, France. While allall agriculturalagricultural weeds weeds compete compete with with crops crops for for the the space space to obtain to obtain water, water, nutrients, nutrients, and light,and parasiticlight, parasitic weeds weeds are particularly are particularly noxious noxious since they since also they directly also extractdirectly valuable extract valuable water and water nutrients and nutrientsfrom the hostfrom plant. the host To plant. extract To nutrients extract nutrients from the hostfrom plants, the host parasitic plants, weedsparasitic have weeds evolved have aevolved unique amulticellular unique multicellular structure structure termed the termed haustorium the haustorium that invades that theinvades host, the forms host, connections forms connections with the with host vascularthe host vascular system, and system, withdraws and withdraws its needed its water needed and water nutrients and [ 7nutrients,8]. Successful [7,8]. Successful haustorial connectionhaustorial connectionto the host resultsto the inhost permanent results damagein permanent during damage a large partduring of the a croplarge life part cycle, of the decreasing crop life the cycle, crop valuedecreasing by reducing the crop the value harvested by reducing yield and the contaminating harvested yield it withand contaminating parasitic seeds. it Worldwide with parasitic expansion seeds. Worldwideof these noxious expansion plant of pests these including noxious theplant widely pests recognizedincluding the genera widelyStriga recognized, Orobanche genera/Phelipanche Striga,, Orobanche/Phelipancheand Cuscuta has become, and a threatCuscuta to has food become security a [threat9]. to food security [9]. There are few sources of crop resistance to parasiticparasitic plant infection [[10,11].10,11]. The identified identified forms of resistance resistance are are classified classified as as pre-attachment pre-attachment or orpost-attachment post-attachment resistance resistance according according to whether to whether the resistancethe resistance occurs occurs before before or orafter after the the haustorium haustorium attaches attaches the the host host surface surface [10]. [10]. Once Once the the crop crop is infected, it is difficult difficult to fend ooffff thethe exhaustionexhaustion of nutrients created by the attached parasite. Then, Then, chemical control is the most frequent commercial method, albeit its application needs to observe specificspecific recommendations for each parasitic lifelife formform [[12].12]. In this review, wewe describedescribe the currentcurrent state of knowledge on the mechanisms controlling the infection process of parasitic weeds, and the defens defensee systems and protection strategies employed by their hosts. Plants 2020, 9, 1184 3 of 26 2. InfectionPlants 2020 by, 9, xParasitic FOR PEER REVIEW Weeds 3 of 26 2.All Infection forms ofby parasiticParasitic Weeds weeds, facultative or obligate parasites, hemiparasites or holoparasites, root parasites, or stem parasites interact with the host crop by means of the haustorium [7]. Two main All forms of parasitic weeds, facultative or obligate parasites, hemiparasites or holoparasites, types of haustoria exist in root parasitic plants [1,8]. The terminal haustorium is typically developed root parasites, or stem parasites interact with the host crop by means of the haustorium [7]. Two main by obligatedtypes of haustoria parasitic exist weeds in root at the parasitic tip oftheir plants embryonic [1,8]. The terminal radicle. haustorium The lateral is haustorium typically developed is developed as anby extension obligated inparasitic hemiparasitic weeds at the radicle tip of and their mature embryonic roots radicle. of hemiparasitic The lateral haustorium and holoparasitic is developed weeds. In abovegroundas an extension parasitic in hemiparasitic weeds that radicle infect and crop mature stems roots and of leaves, hemiparasitic lateral haustoriaand holoparasitic develop weeds. as lateral extensionsIn aboveground of their parasiticparasitic weeds stems that (Figure infect2 ).crop The stems formation and leaves, of a lateral mature haustoria haustorium develop involves as lateral four developmentalextensions of stages: their parasitic Haustorium stems initiation,(Figure 2). hostThe formation invasion, of establishment a mature haustorium of host-parasite involves vascularfour continuity,developmental and the stages: creation Haustorium of a parasitic initiation, sink host that invasion, will be establishment accepted by theof host-parasite crop as one vascular of its own. Severalcontinuity, mechanisms and the of creation crop location of a parasitic adapt sink the that timing will ofbe haustoriumaccepted by the development crop as one toof theits own. resource availabilitySeveral ofmechanisms its hosts[ 13of ].crop location adapt the timing of haustorium development to the resource availability of its hosts [13]. Figure 2. Haustorial
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