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      Host-parasite tissue adhesion by a secreted type of β-1,4-glucanase in the parasitic plant Phtheirospermum japonicum

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          Abstract

          Tissue adhesion between plant species occurs both naturally and artificially. Parasitic plants establish intimate relationship with host plants by adhering tissues at roots or stems. Plant grafting, on the other hand, is a widely used technique in agriculture to adhere tissues of two stems. Here we found that the model Orobanchaceae parasitic plant Phtheirospermum japonicum can be grafted on to interfamily species. To understand molecular basis of tissue adhesion between distant plant species, we conducted comparative transcriptome analyses on both infection and grafting by P. japonicum on Arabidopsis. Despite different organs, we identified the shared gene expression profile, where cell proliferation- and cell wall modification-related genes are up-regulated. Among genes commonly induced in tissue adhesion between distant species, we showed a gene encoding a secreted type of β-1,4-glucanase plays an important role for plant parasitism. Our data provide insights into the molecular commonality between parasitism and grafting in plants.

          Abstract

          Ken-ichi Kurotani, Takanori Wakatake et al. study tissue adhesion in plants. They found that the model Orobanchaceae parasitic plant Phtheirospermum japonicum can be grafted on to interfamily species. Using transcriptome profiling, the identify genes involved in tissue adhesion between distant species and demonstrate that β-1,4-glucanase plays an important role in plant parasitism.

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          Most cited references38

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          A golden gate modular cloning toolbox for plants.

          Plant Synthetic Biology requires robust and efficient methods for assembling multigene constructs. Golden Gate cloning provides a precision module-based cloning technique for facile assembly of multiple genes in one construct. We present here a versatile resource for plant biologists comprising a set of cloning vectors and 96 standardized parts to enable Golden Gate construction of multigene constructs for plant transformation. Parts include promoters, untranslated sequences, reporters, antigenic tags, localization signals, selectable markers, and terminators. The comparative performance of parts in the model plant Nicotiana benthamiana is discussed.
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            The evolution of parasitism in plants.

            The multiple independent origins of plant parasitism suggest that numerous ancestral plant lineages possessed the developmental flexibility to meet the requirements of a parasitic life style, including such adaptations as the ability to recognize host plants, form an invasive haustorium, and regulate the transfer of nutrients and other molecules between two different plants. In this review, we focus on the Orobanchaceae, which are unique among the parasitic plants in that extant member species include the full range of host dependence from facultative to obligate parasites. The recent emergence of genomic resources for these plants should provide new insights into parasitic plant evolution and enable the development of novel genetic strategies for controlling parasitic weeds.
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              PLANT EVOLUTION. Convergent evolution of strigolactone perception enabled host detection in parasitic plants.

              Obligate parasitic plants in the Orobanchaceae germinate after sensing plant hormones, strigolactones, exuded from host roots. In Arabidopsis thaliana, the α/β-hydrolase D14 acts as a strigolactone receptor that controls shoot branching, whereas its ancestral paralog, KAI2, mediates karrikin-specific germination responses. We observed that KAI2, but not D14, is present at higher copy numbers in parasitic species than in nonparasitic relatives. KAI2 paralogs in parasites are distributed into three phylogenetic clades. The fastest-evolving clade, KAI2d, contains the majority of KAI2 paralogs. Homology models predict that the ligand-binding pockets of KAI2d resemble D14. KAI2d transgenes confer strigolactone-specific germination responses to Arabidopsis thaliana. Thus, the KAI2 paralogs D14 and KAI2d underwent convergent evolution of strigolactone recognition, respectively enabling developmental responses to strigolactones in angiosperms and host detection in parasites.
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                Author and article information

                Contributors
                ken.shirasu@riken.jp
                notaguchi.michitaka@b.mbox.nagoya-u.ac.jp
                Journal
                Commun Biol
                Commun Biol
                Communications Biology
                Nature Publishing Group UK (London )
                2399-3642
                30 July 2020
                30 July 2020
                2020
                : 3
                : 407
                Affiliations
                [1 ]GRID grid.27476.30, ISNI 0000 0001 0943 978X, Bioscience and Biotechnology Center, , Nagoya University, ; Furo-cho, Chikusa-ku, Nagoya 464-8601 Japan
                [2 ]GRID grid.26999.3d, ISNI 0000 0001 2151 536X, Graduate School of Science, , The University of Tokyo, ; Bunkyo-ku, Tokyo 113-8657 Japan
                [3 ]GRID grid.7597.c, ISNI 0000000094465255, Center for Sustainable Resource Science, , RIKEN, Tsurumi, ; Yokohama, Kanagawa 230-0045 Japan
                [4 ]GRID grid.27476.30, ISNI 0000 0001 0943 978X, Graduate School of Bioagricultural Sciences, , Nagoya University, ; Furo-cho, Chikusa-ku, Nagoya 464-8601 Japan
                [5 ]GRID grid.260493.a, ISNI 0000 0000 9227 2257, Institute for Research Initiatives, Division for Research Strategy, , Nara Institute of Science and Technology, ; Ikoma, Nara 630-0192 Japan
                [6 ]GRID grid.254217.7, ISNI 0000 0000 8868 2202, College of Bioscience and Biotechnology, , Chubu University, ; Matsumoto-cho, Kasugai 487-8501 Japan
                [7 ]GRID grid.27476.30, ISNI 0000 0001 0943 978X, Institute of Transformative Bio-Molecules, , Nagoya University, ; Furo-cho, Chikusa-ku, Nagoya 464-8601 Japan
                [8 ]GRID grid.8379.5, ISNI 0000 0001 1958 8658, Present Address: Biocenter, Institute for Molecular Plant Physiology and Biophysics, Julius‐von‐Sachs‐Institute, , University of Würzburg, ; 97082 Würzburg, Germany
                [9 ]Present Address: RIKEN BioResource Research Center, Tsukuba, Ibaraki 305-0074 Japan
                Author information
                http://orcid.org/0000-0001-7777-6681
                http://orcid.org/0000-0002-1977-0510
                http://orcid.org/0000-0003-0831-2108
                Article
                1143
                10.1038/s42003-020-01143-5
                7393376
                32733024
                0b39bc81-7e69-4517-aa54-e9e516235fe4
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 11 May 2020
                : 10 July 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/501100001691, MEXT | Japan Society for the Promotion of Science (JSPS);
                Award ID: 15H05959
                Award ID: 17H06172
                Award ID: 18KT0040
                Award ID: 18H03950
                Award ID: 19H05361
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100007132, Cannon Foundation (The Cannon Foundation);
                Award ID: R17-0070
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/501100002241, MEXT | Japan Science and Technology Agency (JST);
                Award ID: START15657559
                Award ID: PRESTO15665754
                Award Recipient :
                Categories
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                © The Author(s) 2020

                molecular biology,plant sciences
                molecular biology, plant sciences

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