Reactive Oxygen Species (ROS) Generation Is Indispensable for Haustorium Formation of the Root Parasitic Plant Striga hermonthica

The parasitic witchweed Striga hermonthica causes devastating damage to crops in sub-Saharan Africa, yet the mechanism of its parasitism is not well understood. Parasitic plants form a special organ called a haustorium to obtain water and nutrients from host plants. The haustorium is induced by host-derived small molecules, collectively named haustorium-inducing factors (HIFs). The most active HIF known to date is 2,6-dimethoxy-p-benzoquinone (DMBQ), originally isolated from sorghum root extracts. It has been suggested that DMBQ is produced by oxidation of its precursor, syringic acid, and that reactive oxygen species (ROS) and peroxidases are involved in the process. However, the roles of ROS in haustorium formation after HIF recognition remain to be elucidated. Here, we investigated the effects of various inhibitors of ROS and ROS-regulating enzymes on haustorium formation in S. hermonthica. Inhibitors of NADPH oxidases and peroxidases inhibited haustorium formation during treatment with DMBQ, syringic acid, and host root extracts, suggesting that ROS production and/or regulation via NADPH oxidases and peroxidases are essential for haustorium formation. We observed hydrogen peroxide accumulation in the haustorium upon treatment with various HIFs. Our results suggest that ROS and ROS-regulating enzymes are indispensable in downstream signaling of HIFs for haustorium formation.

[1]  T. Umezawa,et al.  Host lignin composition affects haustorium induction in the parasitic plants Phtheirospermum japonicum and Striga hermonthica. , 2018, The New phytologist.

[2]  Andrew G. Palmer,et al.  Redox-mediated quorum sensing in plants , 2017, PloS one.

[3]  Jian-Min Zhou,et al.  Apoplastic ROS signaling in plant immunity. , 2017, Current opinion in plant biology.

[4]  S. Yoshida,et al.  Quinone oxidoreductase 2 is involved in haustorium development of the parasitic plant Phtheirospermum japonicum , 2017, Plant signaling & behavior.

[5]  R. Mittler.  ROS Are Good. , 2017, Trends in plant science.

[6]  Andrew G. Palmer,et al.  Detection and Adaptation in Parasitic Angiosperm Host Selection , 2016 .

[7]  S. Yoshida,et al.  The Haustorium, a Specialized Invasive Organ in Parasitic Plants. , 2016, Annual review of plant biology.

[8]  Y. Tsutsumi,et al.  Diverse functions and reactions of class III peroxidases. , 2016, The New phytologist.

[9]  S. Yoshida,et al.  Haustorial Hairs Are Specialized Root Hairs That Support Parasitism in the Facultative Parasitic Plant Phtheirospermum japonicum1[OPEN] , 2015, Plant Physiology.

[10]  C. Zipfel,et al.  Regulation of the NADPH Oxidase RBOHD During Plant Immunity. , 2015, Plant & cell physiology.

[11]  A. Roychoudhury,et al.  Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants , 2014, Front. Environ. Sci..

[12]  S. Yoshida,et al.  Plants that attack plants: molecular elucidation of plant parasitism. , 2012, Current opinion in plant biology.

[13]  Yi-Hsuan Chen,et al.  Heme oxygenase is involved in H2O2-induced lateral root formation in apocynin-treated rice , 2012, Plant Cell Reports.

[14]  Won-Gyu Choi,et al.  In vivo imaging of Ca2+, pH, and reactive oxygen species using fluorescent probes in plants. , 2011, Annual review of plant biology.

[15]  Kentaro Inoue,et al.  A Single-Electron Reducing Quinone Oxidoreductase Is Necessary to Induce Haustorium Development in the Root Parasitic Plant Triphysaria[C][W] , 2010, Plant Cell.

[16]  D. Schachtman,et al.  A peroxidase contributes to ROS production during Arabidopsis root response to potassium deficiency. , 2010, Molecular plant.

[17]  S. Yoshida,et al.  Multiple layers of incompatibility to the parasitic witchweed, Striga hermonthica. , 2009, The New phytologist.

[18]  E. Weeks,et al.  Semagenesis and the parasitic angiosperm Striga asiatica. , 2007, The Plant journal : for cell and molecular biology.

[19]  G. Ejeta.  THE STRIGA SCOURGE IN AFRICA: A GROWING PANDEMIC , 2007 .

[20]  C. Dunand,et al.  Distribution of superoxide and hydrogen peroxide in Arabidopsis root and their influence on root development: possible interaction with peroxidases. , 2007, The New phytologist.

[21]  M. Sagi,et al.  Production of Reactive Oxygen Species by Plant NADPH Oxidases1 , 2006, Plant Physiology.

[22]  J. Slate,et al.  A novel form of resistance in rice to the angiosperm parasite Striga hermonthica. , 2006, The New phytologist.

[23]  J. Blaustein,et al.  Production of Reactive Oxygen Species by Plant NADPH Oxidases1 , 2006, Plant Physiology.

[24]  D. Lynn,et al.  The haustorium and the chemistry of host recognition in parasitic angiosperms , 1986, Journal of Chemical Ecology.

[25]  P. Schopfer,et al.  Production of Reactive Oxygen Intermediates (O2˙−, H2O2, and ˙OH) by Maize Roots and Their Role in Wall Loosening and Elongation Growth , 2004, Plant Physiology.

[26]  P. Zimmermann,et al.  GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox1[w] , 2004, Plant Physiology.

[27]  Tom Misteli,et al.  In vivo imaging. , 2003, Methods.

[28]  R. Apkarian,et al.  Dancing together. Social controls in parasitic plant development. , 2001, Plant physiology.

[29]  R. O’Malley,et al.  Expansin Message Regulation in Parasitic Angiosperms: Marking Time in Development , 2000, Plant Cell.

[30]  R. O’Malley,et al.  Signaling Organogenesis in Parasitic Angiosperms: Xenognosin Generation, Perception, and Response , 2000, Journal of Plant Growth Regulation.

[31]  K. Mori,et al.  Synthesis of (+)‐Strigol and (+)‐Orobanchol, the Germination Stimulants, and Their Stereoisomers by Employing Lipase‐Catalyzed Asymmetric Acetylationas the Key Step , 1999 .

[32]  Phillips,et al.  Flavonoids promote haustoria formation in the root parasite triphysaria versicolor , 1999, Plant physiology.

[33]  L. Boone,et al.  On becoming a parasite: evaluating the role of wall oxidases in parasitic plant development. , 1998, Chemistry & biology.

[34]  R. O’Malley,et al.  A mechanism for inducing plant development: the genesis of a specific inhibitor. , 1996, Proceedings of the National Academy of Sciences of the United States of America.