Plant-parasitic nematode infections in rice: molecular and cellular insights.

Being one of the major staple foods in the world, and an interesting model monocot plant, rice (Oryza sativa L.) has recently received attention from molecular nematologists studying the cellular and molecular aspects of the interaction between this crop and plant-parasitic nematodes. In this review, we highlight recent advances in this field, with a focus on the best-studied root-knot nematodes. Histological studies have revealed the cellular changes inside root-knot nematode-induced feeding sites, both in the compatible interaction with Oryza sativa and the incompatible interaction with the related species Oryza glaberrima. After comparing the published data from transcriptome analyses, mutant studies, and exogenous hormone applications, we provide a comprehensive model showing the role and interaction of plant hormone pathways in defense of this monocot crop against root nematodes, where jasmonate seems to play a key role. Finally, recent evidence indicates that effectors secreted from rice-infecting nematodes can suppress plant defense.

[1]  M. Luc,et al.  Heterodera Sacchari N. Sp. (Nematoda: Tylenchoidea) Parasite De La Canne à Sucre Au Congo-Brazzaville , 1963 .

[2]  J. Seinhorst,et al.  Interaction of Pratylenchus penetrans and Fusarium oxysporum forma pisi race 2 and of Rotylenchus uniformis and F. oxysporum F. pisi race 1 on peas , 1971 .

[3]  C. S. Huang,et al.  Bionomics of white-tip nematode, Aphelenchoides besseyi in rice florets and developing grains. , 1972 .

[4]  I. Ibrahim,et al.  Host-parasite relationship od Meloidogyne incognita (Kofoid et White) Chitw. on rice , 1973 .

[5]  Y. Ohshima Heterodera elachista n.sp., an upland rice cyst nematode from Japan. , 1974 .

[6]  Y. Rao,et al.  Nature of resistance in rice (Oryza sativa L) to the root-knot nematode (Meloidogyne graminicola Golden and Birchfield) II. Histopathology of nematode infection in rice varieties , 1977, Proceedings / Indian Academy of Sciences.

[7]  R. Fortuner,et al.  Root-parasitic nematodes of rice. , 1979 .

[8]  R. T. Mckinley,et al.  Effects of Pratylenchus penetrans on development of strawberry wilt caused by Verticillium dahliae. , 1979 .

[9]  J. Babatola Reactions of some rice cultivars to the root-knot nematode, Meloidogyne incognita. , 1980 .

[10]  J. Bridge,et al.  Feeding Behaviour and Histopathology of Hirschmanniella oryzae, H. imamuri, and H. spinicaudata on Rice. , 1980, Journal of nematology.

[11]  A. Jayaprakash,et al.  Life history and behaviour of the cyst nematode,Heterodera oryzicola Rao and Jayaprakash, 1978 in Rice (Oryza sativa L.) , 1982 .

[12]  J. Bridge,et al.  The rice root-knot nematode, Meloidogyne graminicola, on deep water rice (Oryza sativa subsp. indica). , 1982 .

[13]  J. Babatola Pathogenicity of Heterodera sacchari on rice , 1983 .

[14]  J. P. Hollis,et al.  Occurrence of Aphelenchoides besseyi in Louisiana Rice Seed and Its Interaction with Sclerotium oryzae in Selected Cultivars. , 1984, Journal of nematology.

[15]  J. P. Hollis,et al.  Nematode parasites of rice. , 1984 .

[16]  M. Diomandé Response of upland rice cultivars to Meloidogyne species , 1984 .

[17]  D. Waele,et al.  Effects of Root-Lesion Nematodes (Pratylenchus Brachyur Us Godfrey and P. Zeae Graham) and Fusarium Moniliforme Sheldon Alone or in Combination, On Maize , 1987 .

[18]  D. Freckman,et al.  A world perspective on nematology : The role of the society , 1987 .

[19]  T. Mew,et al.  The effect of Pratylenchus zeae on the growth and yield of upland rice. , 1990 .

[20]  John Bridge,et al.  Nematode parasites of rice. , 1990 .

[21]  E. Kondo,et al.  Growth and Reproductive Parameters of the Rice Stem Nematode Ditylenchus angustus on Botrytis cinerea , 1995 .

[22]  J. Prot,et al.  Effects of Water Regime On the Distribution of Meloidogyne Graminicola and Other Root-Parasitic Nematodes in a Rice Field Toposequence and Pathogenicity of M. Graminicola On Rice Cultivar Upl R15 , 1995 .

[23]  J. Prot,et al.  Influence of water management on tolerance of rice cultivars for Meloidogyne graminicola (1) , 1996 .

[24]  K. Barker,et al.  Plant and Nematode Interactions , 1998 .

[25]  P. Castagnone-Sereno,et al.  The pepper resistance genes Me1 and Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection , 1998 .

[26]  Monty P. Jones,et al.  Resistance to the rice nematodes Heterodera sacchari, Meloidogyne graminicola and M. incognita in Oryza glaberrima and O. glaberrima x O. sativa interspecific hybrids , 1999 .

[27]  G. Réversat,et al.  Resistance to rice root-knot nematode Meloidogyne graminicola identified in Oryza longistaminata and O. glaberrima , 1999 .

[28]  D. Coyne,et al.  Heterodera sacchari: field population dynamics and damage to upland rice in Côte d'Ivoire , 2000 .

[29]  T. Ait-Ali,et al.  HOW GIBBERELLIN REGULATES PLANT GROWTH AND DEVELOPMENT: A Molecular Genetic Analysis of Gibberellin Signaling. , 2001, Annual review of plant physiology and plant molecular biology.

[30]  I. Graham,et al.  Plastid redox state and sugars: interactive regulators of nuclear-encoded photosynthetic gene expression. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[31]  O. Linares African rice (Oryza glaberrima): History and future potential , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  M. Lorieux,et al.  Linkage mapping of Hsa-1Og, a resistance gene of African rice to the cyst nematode, Heterodera sacchari , 2003, Theoretical and Applied Genetics.

[33]  G. Réversat,et al.  Management of Meloidogyne graminicola and yield of upland rice in South-Luzon, Philippines , 2003 .

[34]  I. Baldwin,et al.  Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations. , 2004, The Plant journal : for cell and molecular biology.

[35]  F. Grundler,et al.  Formation of wall openings in root cells of Arabidopsis thaliana following infection by the plant-parasitic nematode Heterodera schachtii , 1998, European Journal of Plant Pathology.

[36]  John T Jones,et al.  A family of glycosyl hydrolase family 45 cellulases from the pine wood nematode Bursaphelenchus xylophilus , 2004, FEBS letters.

[37]  Woong June Park,et al.  From weeds to crops: genetic analysis of root development in cereals. , 2004, Trends in plant science.

[38]  Michel Luc,et al.  Plant parasitic nematodes in subtropical and tropical agriculture , 2005 .

[39]  M. Luc,et al.  Nematode parasites of cereals. , 2005 .

[40]  M. Nicole,et al.  Hypersensitive-like reaction conferred by the Mex-1 resistance gene against Meloidogyne exigua in coffee , 2005 .

[41]  Frédérique Bitton,et al.  Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. , 2005, The Plant journal : for cell and molecular biology.

[42]  C. Vijayakumar,et al.  ROOT-KNOT NEMATODE RESISTANCE IN ADVANCED BACK CROSS POPULATIONS OF RICE DEVELOPED FOR WATER STRESS CONDITIONS , 2006 .

[43]  A. Elsen,et al.  Challenges in tropical plant nematology. , 2007, Annual review of phytopathology.

[44]  A. Price,et al.  Physiological and genetic mapping study of tolerance to root-knot nematode in rice. , 2007, The New phytologist.

[45]  P. Gantet,et al.  Molecular Genetics of Rice Root Development , 2009, Rice.

[46]  Jonathan D. G. Jones,et al.  DELLAs Control Plant Immune Responses by Modulating the Balance of Jasmonic Acid and Salicylic Acid Signaling , 2008, Current Biology.

[47]  J. McCarter Molecular Approaches Toward Resistance to Plant-Parasitic Nematodes , 2008 .

[48]  J. Vogel Unique aspects of the grass cell wall. , 2008, Current opinion in plant biology.

[49]  M. Sié,et al.  Molecular profiling of interspecific lowland rice populations derived from IR64 ( Oryza sativa ) and Tog5681 ( Oryza glaberrima ) , 2008 .

[50]  T. Maier,et al.  Arabidopsis small RNAs and their targets during cyst nematode parasitism. , 2008, Molecular plant-microbe interactions : MPMI.

[51]  M. Moens,et al.  Migratory plant endoparasitic nematodes: a group rich in contrasts and divergence. , 2009, Annual review of phytopathology.

[52]  B. Bouman,et al.  Biotic and abiotic causes of yield failure in tropical aerobic rice. , 2009 .

[53]  M. Moens,et al.  Hatch and host location. , 2009 .

[54]  G. Réversat,et al.  Evaluation of Oryza sativa x O. glaberrima derived progenies for resistance to rootknot nematode and identification of introgressed alien chromosome segments using SSR markers , 2010 .

[55]  M. F. Grossi-de-Sá,et al.  Resistance to Meloidogyne incognita expresses a hypersensitive-like response in Coffea arabica , 2010, European Journal of Plant Pathology.

[56]  T. Lwin,et al.  Occurrence of the rice root nematode Hirschmanniella oryzae on monsoon rice in Myanmar , 2010 .

[57]  S. Powers,et al.  Comparison of host recognition, invasion, development and reproduction of Meloidogyne graminicola and M. incognita on rice and tomato , 2011 .

[58]  D. Esmenjaud,et al.  Histological mechanisms of the resistance conferred by the Ma gene against Meloidogyne incognita in Prunus spp. , 2011, Phytopathology.

[59]  G. Gheysen,et al.  How nematodes manipulate plant development pathways for infection. , 2011, Current opinion in plant biology.

[60]  M. Mckenry,et al.  Rice-root nematode, Hirschmaniella oryzae, infecting rice selections and weed genotypes , 2011 .

[61]  G. Gheysen,et al.  The Jasmonate Pathway Is a Key Player in Systemically Induced Defense against Root Knot Nematodes in Rice1[C] , 2011, Plant Physiology.

[62]  D. Waele,et al.  Effect of agro-ecosystem on the occurrence of the rice root-knot nematode Meloidogyne graminicola on rice in Myanmar , 2011, Australasian Plant Pathology.

[63]  C. Pieterse,et al.  Hormonal modulation of plant immunity. , 2012, Annual review of cell and developmental biology.

[64]  D. Peng,et al.  First Report of the Cyst Nematode (Heterodera elachista) on Rice in Hunan Province, China. , 2012, Plant disease.

[65]  S. Powers,et al.  Effect of small lipophilic molecules in tomato and rice root exudates on the behaviour of Meloidogyne incognita and M. graminicola , 2012 .

[66]  G. Gheysen,et al.  Comparing systemic defence-related gene expression changes upon migratory and sedentary nematode attack in rice. , 2012, Plant biology.

[67]  Arvind Kumar,et al.  Comparison of migration, penetration, development and reproduction of Meloidogyne graminicola on susceptible and resistant rice genotypes , 2012 .

[68]  Wei Dong,et al.  Identification of Soybean MicroRNAs Involved in Soybean Cyst Nematode Infection by Deep Sequencing , 2012, PloS one.

[69]  G. Gheysen,et al.  Transcriptional reprogramming by root knot and migratory nematode infection in rice. , 2012, The New phytologist.

[70]  M. Wopereis,et al.  Crops that feed the world 7: Rice , 2012, Food Security.

[71]  G. Gheysen,et al.  Abscisic acid interacts antagonistically with classical defense pathways in rice-migratory nematode interaction. , 2012, The New phytologist.

[72]  S. Kikuchi,et al.  Brassinosteroids Antagonize Gibberellin- and Salicylate-Mediated Root Immunity in Rice1[C][W][OA] , 2012, Plant Physiology.

[73]  D. Nettleton,et al.  The Arabidopsis MicroRNA396-GRF1/GRF3 Regulatory Module Acts as a Developmental Regulator in the Reprogramming of Root Cells during Cyst Nematode Infection1[W][OA] , 2012, Plant Physiology.

[74]  Chao Zhang,et al.  Molecular Characterization and Functions of Fatty Acid and Retinoid Binding Protein Gene (Ab-far-1) in Aphelenchoides besseyi , 2013, PloS one.

[75]  G. Gheysen,et al.  Brassinosteroids suppress rice defense against root-knot nematodes through antagonism with the jasmonate pathway. , 2013, Molecular plant-microbe interactions : MPMI.

[76]  H. Fourie,et al.  Comparative cellular responses in susceptible and resistant soybean cultivars infected by Meloidogyne incognita , 2013 .

[77]  G. Gheysen,et al.  Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots , 2013, Journal of experimental botany.

[78]  A. Troccoli,et al.  Heterodera elachista the Japanese cyst nematode parasitizing corn in Northern Italy: integrative diagnosis and bionomics , 2013, European Journal of Plant Pathology.

[79]  R. Togawa,et al.  Transcription profile of soybean-root-knot nematode interaction reveals a key role of phythormones in the resistance reaction , 2013, BMC Genomics.

[80]  T. Baum,et al.  Manipulation of plant cells by cyst and root-knot nematode effectors. , 2013, Molecular plant-microbe interactions : MPMI.

[81]  P. Urwin,et al.  Identification of Genes Involved in the Response of Arabidopsis to Simultaneous Biotic and Abiotic Stresses1[C][W][OPEN] , 2013, Plant Physiology.

[82]  G. Gheysen,et al.  Identification of candidate effector genes in the transcriptome of the rice root knot nematode Meloidogyne graminicola. , 2013, Molecular plant pathology.

[83]  K. Lindsey,et al.  Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: a functional role for gene repression. , 2013, The New phytologist.

[84]  Godelieve Gheysen,et al.  Hormone defense networking in rice: tales from a different world. , 2013, Trends in plant science.

[85]  D. Waele,et al.  Population dynamics of Meloidogyne graminicola and Hirschmanniella oryzae in a double rice-cropping sequence in the lowlands of Myanmar , 2013 .

[86]  G. Gheysen,et al.  Nematode feeding sites: unique organs in plant roots , 2013, Planta.

[87]  P. Abad,et al.  The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. , 2013, Molecular plant-microbe interactions : MPMI.

[88]  M. Moens,et al.  Migratory endoparasitic nematodes. , 2013 .

[89]  Johannes Helder,et al.  Top 10 plant-parasitic nematodes in molecular plant pathology. , 2013, Molecular plant pathology.

[90]  Ionit Iberkleid,et al.  Fatty Acid-and Retinol-Binding Protein, Mj-FAR-1 Induces Tomato Host Susceptibility to Root-Knot Nematodes , 2013, PloS one.

[91]  Vu Phong Nguyen Caractérisation d’effecteurs de virulence du nématode à galles Meloidogyne incognita chez le riz (Oryza sativa) , 2013 .

[92]  L. Fernandez,et al.  Life cycle of the rice root-knot nematode Meloidogyne graminicola at different temperatures under non-flooded and flooded conditions , 2014 .

[93]  Peter J. A. Cock,et al.  Characterisation of the transcriptome of Aphelenchoides besseyi and identification of a GHF 45 cellulase , 2014 .

[94]  Arvind Kumar,et al.  Histopathology of the rice root-knot nematode, Meloidogyne graminicola, on Oryza sativa and O. glaberrima , 2014 .

[95]  G. Gheysen,et al.  Analysis of the transcriptome of Hirschmanniella oryzae to explore potential survival strategies and host-nematode interactions. , 2014, Molecular plant pathology.

[96]  P. Gantet,et al.  Meloidogyne incognita - rice (Oryza sativa) interaction: a new model system to study plant-root-knot nematode interactions in monocotyledons , 2014, Rice.