Integration of danger peptide signals with herbivore-associated molecular pattern signaling amplifies anti-herbivore defense responses in rice

被引:34
作者
Shinya, Tomonori [1 ]
Yasuda, Shigetaka [2 ]
Hyodo, Kiwamu [1 ]
Tani, Rena [2 ]
Hojo, Yuko [1 ]
Fujiwara, Yuka [1 ]
Hiruma, Kei [2 ,3 ]
Ishizaki, Takuma [4 ]
Fujita, Yasunari [5 ,6 ]
Saijo, Yusuke [2 ,3 ]
Galis, Ivan [1 ]
机构
[1] Okayama Univ, Inst Plant Sci & Resources, Kurashiki, Okayama 7100046, Japan
[2] Nara Inst Sci & Technol, Grad Sch Biol Sci, Ikoma, Nara 6300192, Japan
[3] JST, Precursory Res Embryon Sci & Technol PRESTO, Kawaguchi, Saitama 3320012, Japan
[4] JIRCAS, Trop Agr Res Front, Ishigaki, Okinawa 9070002, Japan
[5] JIRCAS, Biol Resources & Post Harvest Div, Tsukuba, Ibaraki 3058686, Japan
[6] Univ Tsukuba, Grad Sch Life & Environm Sci, Tsukuba, Ibaraki 3058572, Japan
关键词
plant-herbivore interactions; danger-associated molecular patterns; herbivore-associated molecular patterns; synergistic effects; plant immunity; rice; Oryza sativa; OsPeps; PLANT ELICITOR PEPTIDES; INNATE IMMUNE-RESPONSE; ORYZA-SATIVA; NICOTIANA-ATTENUATA; ARABIDOPSIS; RECEPTOR; RECOGNITION; BIOSYNTHESIS; CONTRIBUTES; CELLS;
D O I
10.1111/tpj.13883
中图分类号
Q94 [植物学];
学科分类号
071001 ;
摘要
Plant defense against herbivores is modulated by herbivore-associated molecular patterns (HAMPs) from oral secretions (OS) and/or saliva of insects. Furthermore, feeding wounds initiate plant self-damage responses modulated by danger-associated molecular patterns (DAMPs) such as immune defense-promoting plant elicitor peptides (Peps). While temporal and spatial co-existence of both patterns during herbivory implies a possibility of their close interaction, the molecular mechanisms remain undetermined. Here we report that exogenous application of rice (Oryza sativa) peptides (OsPeps) can elicit multiple defense responses in rice cell cultures. Specific activation of OsPROPEP3 gene transcripts in rice leaves by wounding and OS treatments further suggests a possible involvement of the OsPep3 peptide in rice-herbivore interactions. Correspondingly, we found that simultaneous application of OsPep3 and Mythimna loreyi OS significantly amplifies an array of defense responses in rice cells, including mitogen-activated protein kinase activation, and generation of defense-related hormones and metabolites. The induction of OsPROPEP3/4 by OsPep3 points to a positive auto-feedback loop in OsPep signaling which may contribute to additional enhancement of defense signal(s). Finally, the overexpression of the OsPep receptor OsPEPR1 increases the sensitivity of rice plants not only to the cognate OsPeps but also to OS signals. Our findings collectively suggest that HAMP-DAMP signal integration provides a critical step in the amplification of defense signaling in plants.
引用
收藏
页码:626 / 637
页数:12
相关论文
共 41 条
[1]   Cues from chewing insects - the intersection of DAMPs, HAMPs, MAMPs and effectors [J].
Acevedo, Flor E. ;
Rivera-Vega, Loren J. ;
Chung, Seung Ho ;
Ray, Swayamjit ;
Felton, Gary W. .
CURRENT OPINION IN PLANT BIOLOGY, 2015, 26 :80-86
[2]   Systematic analysis of rice (Oryza sativa) metabolic responses to herbivory [J].
Alamgir, Kabir Md ;
Hojo, Yuko ;
Christeller, John T. ;
Fukumoto, Kaori ;
Isshiki, Ryutaro ;
Shinya, Tomonori ;
Baldwin, Ian T. ;
Galis, Ivan .
PLANT CELL AND ENVIRONMENT, 2016, 39 (02) :453-466
[3]   The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses [J].
Bartels, Sebastian ;
Lori, Martina ;
Mbengue, Malick ;
van Verk, Marcel ;
Klauser, Dominik ;
Hander, Tim ;
Boeni, Rainer ;
Robatzek, Silke ;
Boller, Thomas .
JOURNAL OF EXPERIMENTAL BOTANY, 2013, 64 (17) :5309-5321
[4]   Self-regulation and cross-regulation of pattern-recognition receptor signalling in health and disease [J].
Cao, Xuetao .
NATURE REVIEWS IMMUNOLOGY, 2016, 16 (01) :35-50
[5]   Dynamic Plant-Plant-Herbivore Interactions Govern Plant Growth-Defence Integration [J].
de Vries, Jorad ;
Evers, Jochem B. ;
Poelman, Erik H. .
TRENDS IN PLANT SCIENCE, 2017, 22 (04) :329-337
[6]   Sources of specificity in plant damaged-self recognition [J].
Duran-Flores, Dalia ;
Heil, Martin .
CURRENT OPINION IN PLANT BIOLOGY, 2016, 32 :77-87
[7]   Response of Rice to Insect Elicitors and the Role of OsJAR1 in Wound and Herbivory-Induced JA-Ile Accumulation [J].
Fukumoto, Kaori ;
Alamgir, Kabir Md ;
Yamashita, Yuko ;
Mori, Izumi C. ;
Matsuura, Hideyuki ;
Galis, Ivan .
JOURNAL OF INTEGRATIVE PLANT BIOLOGY, 2013, 55 (08) :775-784
[8]   Comparative efficacies in vitro of antibacterial, fungicidal, antioxidant, and herbicidal activities of momilatones A and B [J].
Fukuta, Masakazu ;
Xuan, Tran Dang ;
Deba, Farah ;
Tawata, Shinkichi ;
Khanh, Tran Dang ;
Chung, Ill Min .
JOURNAL OF PLANT INTERACTIONS, 2007, 2 (04) :245-251
[9]   Perception of Arabidopsis AtPep peptides, but not bacterial elicitors, accelerates starvation-induced senescence [J].
Gully, Kay ;
Hander, Tim ;
Boller, Thomas ;
Bartels, Sebastian .
FRONTIERS IN PLANT SCIENCE, 2015, 6 :1-10
[10]   Sensing Danger: Key to Activating Plant Immunity [J].
Gust, Andrea A. ;
Pruitt, Rory ;
Nuernberger, Thorsten .
TRENDS IN PLANT SCIENCE, 2017, 22 (09) :779-791