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      Adaptation of the parasitic plant lifecycle: germination is controlled by essential host signaling molecules

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          Abstract

          Parasitic plants are plants that connect with a haustorium to the vasculature of another, host, plant from which they absorb water, assimilates, and nutrients. Because of this parasitic lifestyle, parasitic plants need to coordinate their lifecycle with that of their host. Parasitic plants have evolved a number of host detection/host response mechanisms of which the germination in response to chemical host signals in one of the major families of parasitic plants, the Orobanchaceae, is a striking example. In this update review, we discuss these germination stimulants. We review the different compound classes that function as germination stimulants, how they are produced, and in which host plants. We discuss why they are reliable signals, how parasitic plants have evolved mechanisms that detect and respond to them, and whether they play a role in host specificity. The advances in the knowledge underlying this signaling relationship between host and parasitic plant have greatly improved our understanding of the evolution of plant parasitism and are facilitating the development of more effective control measures in cases where these parasitic plants have developed into weeds.

          Abstract

          Root parasitic plants grow on the roots of other plants and germinate only in the presence of that host, on which they completely depend, through the perception of host presence signaling molecules called germination stimulants.

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          Most cited references173

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          Plant sesquiterpenes induce hyphal branching in arbuscular mycorrhizal fungi.

          Arbuscular mycorrhizal (AM) fungi form mutualistic, symbiotic associations with the roots of more than 80% of land plants. The fungi are incapable of completing their life cycle in the absence of a host root. Their spores can germinate and grow in the absence of a host, but their hyphal growth is very limited. Little is known about the molecular mechanisms that govern signalling and recognition between AM fungi and their host plants. In one of the first stages of host recognition, the hyphae of AM fungi show extensive branching in the vicinity of host roots before formation of the appressorium, the structure used to penetrate the plant root. Host roots are known to release signalling molecules that trigger hyphal branching, but these branching factors have not been isolated. Here we have isolated a branching factor from the root exudates of Lotus japonicus and used spectroscopic analysis and chemical synthesis to identify it as a strigolactone, 5-deoxy-strigol. Strigolactones are a group of sesquiterpene lactones, previously isolated as seed-germination stimulants for the parasitic weeds Striga and Orobanche. The natural strigolactones 5-deoxy-strigol, sorgolactone and strigol, and a synthetic analogue, GR24, induced extensive hyphal branching in germinating spores of the AM fungus Gigaspora margarita at very low concentrations.
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            Strigolactone inhibition of shoot branching.

            A carotenoid-derived hormonal signal that inhibits shoot branching in plants has long escaped identification. Strigolactones are compounds thought to be derived from carotenoids and are known to trigger the germination of parasitic plant seeds and stimulate symbiotic fungi. Here we present evidence that carotenoid cleavage dioxygenase 8 shoot branching mutants of pea are strigolactone deficient and that strigolactone application restores the wild-type branching phenotype to ccd8 mutants. Moreover, we show that other branching mutants previously characterized as lacking a response to the branching inhibition signal also lack strigolactone response, and are not deficient in strigolactones. These responses are conserved in Arabidopsis. In agreement with the expected properties of the hormonal signal, exogenous strigolactone can be transported in shoots and act at low concentrations. We suggest that endogenous strigolactones or related compounds inhibit shoot branching in plants. Furthermore, ccd8 mutants demonstrate the diverse effects of strigolactones in shoot branching, mycorrhizal symbiosis and parasitic weed interaction.
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              Inhibition of shoot branching by new terpenoid plant hormones.

              Shoot branching is a major determinant of plant architecture and is highly regulated by endogenous and environmental cues. Two classes of hormones, auxin and cytokinin, have long been known to have an important involvement in controlling shoot branching. Previous studies using a series of mutants with enhanced shoot branching suggested the existence of a third class of hormone(s) that is derived from carotenoids, but its chemical identity has been unknown. Here we show that levels of strigolactones, a group of terpenoid lactones, are significantly reduced in some of the branching mutants. Furthermore, application of strigolactones inhibits shoot branching in these mutants. Strigolactones were previously found in root exudates acting as communication chemicals with parasitic weeds and symbiotic arbuscular mycorrhizal fungi. Thus, we propose that strigolactones act as a new hormone class-or their biosynthetic precursors-in regulating above-ground plant architecture, and also have a function in underground communication with other neighbouring organisms.
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                Author and article information

                Journal
                Plant Physiol
                Plant Physiol
                plphys
                Plant Physiology
                Oxford University Press
                0032-0889
                1532-2548
                April 2021
                18 December 2020
                18 December 2020
                : 185
                : 4
                : 1292-1308
                Affiliations
                Plant Hormone Biology group, Green Life Sciences cluster, Swammerdam Institute for Life Science, University of Amsterdam , 1098 XH Amsterdam, The Netherlands
                Author notes
                Author for communication: h.j.bouwmeester@ 123456uva.nl

                Senior author.

                Author information
                https://orcid.org/0000-0003-0907-2732
                https://orcid.org/0000-0002-9579-4127
                https://orcid.org/0000-0001-8653-4799
                https://orcid.org/0000-0002-1435-1907
                Article
                kiaa066
                10.1093/plphys/kiaa066
                8133609
                33793901
                f3450d2a-afcd-43fc-ae61-020cab9a9e24
                © The Author(s) 2020. 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.

                History
                : 21 July 2020
                : 12 November 2020
                Page count
                Pages: 17
                Funding
                Funded by: European Research Council, DOI 10.13039/100010663;
                Award ID: 670211
                Funded by: China Scholarship Council, DOI 10.13039/501100004543;
                Funded by: Bill & Melinda Gates Foundation, DOI 10.13039/100000865;
                Award ID: OPP1082853
                Funded by: Marie Curie fellowship;
                Award ID: 793795
                Categories
                Focus Issue on Parasitic Plants
                Updates
                AcademicSubjects/SCI02286
                AcademicSubjects/SCI02287
                AcademicSubjects/SCI01270
                AcademicSubjects/SCI01280
                AcademicSubjects/SCI02288

                Plant science & Botany
                Plant science & Botany

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