Literature DB >> 28461500

Interspecies hormonal control of host root morphology by parasitic plants.

Thomas Spallek1, Charles W Melnyk2, Takanori Wakatake3,4, Jing Zhang2, Yuki Sakamoto5, Takatoshi Kiba3, Satoko Yoshida6, Sachihiro Matsunaga5,7, Hitoshi Sakakibara3, Ken Shirasu1,4.   

Abstract

Parasitic plants share a common anatomical feature, the haustorium. Haustoria enable both infection and nutrient transfer, which often leads to growth penalties for host plants and yield reduction in crop species. Haustoria also reciprocally transfer substances, such as RNA and proteins, from parasite to host, but the biological relevance for such movement remains unknown. Here, we studied such interspecies transport by using the hemiparasitic plant Phtheirospermum japonicum during infection of Arabidopsis thaliana Tracer experiments revealed a rapid and efficient transfer of carboxyfluorescein diacetate (CFDA) from host to parasite upon formation of vascular connections. In addition, Phtheirospermum induced hypertrophy in host roots at the site of infection, a form of enhanced secondary growth that is commonly observed during various parasitic plant-host interactions. The plant hormone cytokinin is important for secondary growth, and we observed increases in cytokinin and its response during infection in both host and parasite. Phtheirospermum-induced host hypertrophy required cytokinin signaling genes (AHK3,4) but not cytokinin biosynthesis genes (IPT1,3,5,7) in the host. Furthermore, expression of a cytokinin-degrading enzyme in Phtheirospermum prevented host hypertrophy. Wild-type hosts with hypertrophy were smaller than ahk3,4 mutant hosts resistant to hypertrophy, suggesting hypertrophy improves the efficiency of parasitism. Taken together, these results demonstrate that the interspecies movement of a parasite-derived hormone modified both host root morphology and fitness. Several microbial and animal plant pathogens use cytokinins during infections, highlighting the central role of this growth hormone during the establishment of plant diseases and revealing a common strategy for parasite infections of plants.

Entities:  

Keywords:  Arabidopsis; cytokinin; hypertrophy; parasitism; transport

Mesh:

Substances:

Year:  2017        PMID: 28461500      PMCID: PMC5441792          DOI: 10.1073/pnas.1619078114

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.

Authors:  Tomás Werner; Václav Motyka; Valérie Laucou; Rafaël Smets; Harry Van Onckelen; Thomas Schmülling
Journal:  Plant Cell       Date:  2003-10-10       Impact factor: 11.277

2.  Cytokinins are central regulators of cambial activity.

Authors:  Miho Matsumoto-Kitano; Takami Kusumoto; Petr Tarkowski; Kaori Kinoshita-Tsujimura; Katerina Václavíková; Kaori Miyawaki; Tatsuo Kakimoto
Journal:  Proc Natl Acad Sci U S A       Date:  2008-12-11       Impact factor: 11.205

3.  Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts.

Authors:  Gunjune Kim; Megan L LeBlanc; Eric K Wafula; Claude W dePamphilis; James H Westwood
Journal:  Science       Date:  2014-08-15       Impact factor: 47.728

4.  Cytokinins.

Authors:  Joseph J Kieber; G Eric Schaller
Journal:  Arabidopsis Book       Date:  2014-01-02

Review 5.  The Haustorium, a Specialized Invasive Organ in Parasitic Plants.

Authors:  Satoko Yoshida; Songkui Cui; Yasunori Ichihashi; Ken Shirasu
Journal:  Annu Rev Plant Biol       Date:  2016-04-29       Impact factor: 26.379

6.  Haustorial Hairs Are Specialized Root Hairs That Support Parasitism in the Facultative Parasitic Plant Phtheirospermum japonicum.

Authors:  Songkui Cui; Takanori Wakatake; Kei Hashimoto; Simon B Saucet; Kiminori Toyooka; Satoko Yoshida; Ken Shirasu
Journal:  Plant Physiol       Date:  2015-12-28       Impact factor: 8.340

7.  A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants.

Authors:  Shahid Siddique; Zoran S Radakovic; Carola M De La Torre; Demosthenis Chronis; Ondřej Novák; Eswarayya Ramireddy; Julia Holbein; Christiane Matera; Marion Hütten; Philipp Gutbrod; Muhammad Shahzad Anjam; Elzbieta Rozanska; Samer Habash; Abdelnaser Elashry; Miroslaw Sobczak; Tatsuo Kakimoto; Miroslav Strnad; Thomas Schmülling; Melissa G Mitchum; Florian M W Grundler
Journal:  Proc Natl Acad Sci U S A       Date:  2015-09-28       Impact factor: 11.205

8.  A Developmental Framework for Graft Formation and Vascular Reconnection in Arabidopsis thaliana.

Authors:  Charles W Melnyk; Christoph Schuster; Ottoline Leyser; Elliot M Meyerowitz
Journal:  Curr Biol       Date:  2015-04-16       Impact factor: 10.834

9.  Arabidopsis KNOXI proteins activate cytokinin biosynthesis.

Authors:  Osnat Yanai; Eilon Shani; Karel Dolezal; Petr Tarkowski; Robert Sablowski; Goran Sandberg; Alon Samach; Naomi Ori
Journal:  Curr Biol       Date:  2005-09-06       Impact factor: 10.834

10.  Cytokinin Production by the Rice Blast Fungus Is a Pivotal Requirement for Full Virulence.

Authors:  Emilie Chanclud; Anna Kisiala; Neil R J Emery; Véronique Chalvon; Aurélie Ducasse; Corinne Romiti-Michel; Antoine Gravot; Thomas Kroj; Jean-Benoit Morel
Journal:  PLoS Pathog       Date:  2016-02-22       Impact factor: 6.823

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  20 in total

1.  Host sunflower-induced silencing of parasitism-related genes confers resistance to invading Orobanche cumana.

Authors:  Zhengqiang Jiang; Qiqi Zhao; Runyao Bai; Ruonan Yu; Pengfei Diao; Ting Yan; Huimin Duan; Xuesong Ma; Zikai Zhou; Yanyan Fan; Hada Wuriyanghan
Journal:  Plant Physiol       Date:  2021-03-15       Impact factor: 8.340

2.  Parasitic plant, from inside out: endophytic development in Lathrophytum peckoltii (Balanophoraceae) in host liana roots from tribe Paullineae (Sapindaceae).

Authors:  Lauany C O Pellissari; Luiza Teixeira-Costa; Gregorio Ceccantini; Neusa Tamaio; Leandro J T Cardoso; João M A Braga; Claudia F Barros
Journal:  Ann Bot       Date:  2022-02-11       Impact factor: 4.357

3.  Phloem-Conducting Cells in Haustoria of the Root-Parasitic Plant Phelipanche aegyptiaca Retain Nuclei and Are Not Mature Sieve Elements.

Authors:  Minako Ekawa; Koh Aoki
Journal:  Plants (Basel)       Date:  2017-12-05

4.  Induced cell fate transitions at multiple cell layers configure haustorium development in parasitic plants.

Authors:  Takanori Wakatake; Satoko Yoshida; Ken Shirasu
Journal:  Development       Date:  2018-07-23       Impact factor: 6.868

Review 5.  A Pivotal Role of Hormones in Regulating Cotton Fiber Development.

Authors:  Guanghui Xiao; Peng Zhao; Yu Zhang
Journal:  Front Plant Sci       Date:  2019-02-14       Impact factor: 5.753

6.  Subtilase activity in intrusive cells mediates haustorium maturation in parasitic plants.

Authors:  Satoshi Ogawa; Takanori Wakatake; Thomas Spallek; Juliane K Ishida; Ryosuke Sano; Tetsuya Kurata; Taku Demura; Satoko Yoshida; Yasunori Ichihashi; Andreas Schaller; Ken Shirasu
Journal:  Plant Physiol       Date:  2021-04-23       Impact factor: 8.340

7.  Molecular actors of seed germination and haustoriogenesis in parasitic weeds.

Authors:  Guillaume Brun; Thomas Spallek; Philippe Simier; Philippe Delavault
Journal:  Plant Physiol       Date:  2021-04-23       Impact factor: 8.340

8.  Mechanisms of resistance and virulence in parasitic plant-host interactions.

Authors:  Markus Albert; Michael J Axtell; Michael P Timko
Journal:  Plant Physiol       Date:  2021-04-23       Impact factor: 8.340

9.  Molecular dissection of haustorium development in Orobanchaceae parasitic plants.

Authors:  Kaori Miyashima Furuta; Lei Xiang; Songkui Cui; Satoko Yoshida
Journal:  Plant Physiol       Date:  2021-07-06       Impact factor: 8.340

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

Authors:  Ken-Ichi Kurotani; Takanori Wakatake; Yasunori Ichihashi; Koji Okayasu; Yu Sawai; Satoshi Ogawa; Songkui Cui; Takamasa Suzuki; Ken Shirasu; Michitaka Notaguchi
Journal:  Commun Biol       Date:  2020-07-30
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