Plant basal resistance to nematodes: An update

Journal of Experimental Botany

Volumn 67, Issue 7, 2016, Pages 2049-2061

  Holbein, Julia ^a   Grundler, Florian M W ^a   Siddique, Shahid ^a  

^a UNIVERSITY OF BONN   (Germany)

Author keywords

Ascarosides; Basal defence; Callose; Endodermis; Lignin; Nematodes; PAMPS; PTI; ROS; Suberin

Indexed keywords

ANIMAL; IMMUNOLOGY; NEMATODE; PARASITOLOGY; PHYSIOLOGY; PLANT; PLANT DISEASE;

ANIMALS; NEMATODA; PLANT DISEASES; PLANTS;

EID: 84965007051     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erw005     Document Type: Review

References (109)

1. Abad P, Castagnone-Sereno P, Rosso MN, Engler JD, Favery B. 2009. Invasion, feeding and development. In: Abad P, Moens M, Starr JL, eds. Root-knot nematodes . Cambridge: CABI International Press, 163-181.
2. Ali MA, Abbas A, Kreil DP, Bohlmann H. 2013. Overexpression of the transcription factor RAP2.6 leads to enhanced callose deposition in syncytia and enhanced resistance against the beet cyst nematode Heterodera schachtii in Arabidopsis roots. BMC Plant Biology 13, 13-47.
3. Ausubel FM. 2005. Are innate immune signaling pathways in plants and animals conserved? Nature Immunology 6, 973-979.
4. Bagniewska-Zadworna A, Arasimowicz-Jelonek M, Smolinski DJ, Stelmasik A. 2014. New insights into pioneer root xylem development: Evidence obtained from Populus trichocarpa plants grown under field conditions. Annals of Botany 113, 1235-1247.
5. Balhadere P, Evans AAF. 1995. Cytochemical investigation of resistance to root-knot nematode Meloidogyne naasi in cereals and grasses using cryosections of roots. Fundamental and Applied Nematology 18, 539-547.
6. Balic A, Harcus Y, Holland MJ, Maizels RM. 2004. Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. European Journal of Immunology 34, 3047-3059.
7. Barcala M, Garcia A, Cabrera J, Casson S, Lindsey K, Favery B, Garcia-Casado G, Solano R, Fenoll C, Escobar C. 2010. Earlytranscriptomic events in microdissected Arabidopsis nematode-induced giant cells. The Plant Journal 61, 698-712.
8. Baxter I, Hosmani PS, Rus A, et al. 2009. Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genetics 5, e1000492.
9. Benedetti M, Pontiggia D, Raggi S, Cheng ZY, Scaloni F, Ferrari S, Ausubel FM, Cervone F, De Lorenzo G. 2015. Plant immunity triggered by engineered in vivo release of oligogalacturonides, damage- Associated molecular patterns. Proceedings of the National Academy of Sciences, USA 112, 5533-5538.
10. Bhattarai KK, Xie QG, Mantelin S, Bishnoi U, Girke T, Navarre DA, Kaloshian I. 2008. Tomato susceptibility to root-knot nematodes requires an intact jasmonic acid signaling pathway. Molecular Plant-Microbe Interactions 21, 1205-1214.
11. Bishop PD, Makus DJ, Pearce G, Ryan CA. 1981. Proteinase inhibitorinducing factor activity in tomato leaves resides in oligosaccharides enzymically released from cell-walls. Proceedings of the National Academy of Sciences, USA 78, 3536-3540.
12. Boerjan W, Ralph J, Baucher M. 2003. Lignin biosynthesis. Annual Review of Plant Biology 54, 519-546.
13. Bohlmann H, Sobczak M. 2014. The plant cell wall in the feeding sites of cyst nematodes. Frontiers in Plant Science 5, 89.
14. Boller T, Felix G. 2009. A renaissance of elicitors: Perception of microbeassociated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379-406.
15. Bouwmeester K, Govers F. 2009. Arabidopsis L- Type lectin receptor kinases: Phylogeny, classification, and expression profiles. Journal of Experimental Botany 60, 4383-4396.
16. Bouwmeester K, Han M, Blanco-Portales R, Song W, Weide R, Guo LY, van der Vossen EAG, Govers F. 2014. The Arabidopsis lectin receptor kinase LecRK-I.9 enhances resistance to Phytophthora infestans in Solanaceous plants. Plant Biotechnology Journal 12, 10-16.
17. Broekaert WF, Cammue BPA, DeBolle MFC, Thevissen K, DeSamblanx GW, Osborne RW. 1997. Antimicrobial peptides from plants. Critical Reviews in Plant Sciences 16, 297-323.
18. Cervone F, Delorenzo G, Degra L, Salvi G, Bergami M. 1987. Purification and characterization of a polygalacturonase-inhibiting protein from Phaseolus vulgaris L. Plant Physiology 85, 631-637.
19. Cervone F, Hahn MG, Delorenzo G, Darvill A, Albersheim P. 1989. Host-pathogen interactions. XXXII. A plant protein converts a fungal pathogenesis factor into an elicitor of plant defense responses. Plant Physiology 90, 542-548.
20. Chronis D, Chen S, Lu S, Hewezi T, Carpenter SCD, Loria R, Baum TJ, Wang X. 2013. A ubiquitin carboxyl extension protein secreted from a plant-parasitic nematode Globodera rostochiensis is cleaved in planta to promote plant parasitism. The Plant Journal 74, 185-196.
21. Clarke AJ, Cox PM, Shepherd AM. 1967. Chemical composition of the egg shells of the potato cyst-nematode Heterodera rostochiensis Woll. Biochemical Journal 104, 1056-1060.
22. Davies KG, Curtis RHC. 2011. Cuticle surface coat of plant-parasitic nematodes. Annual Review of Phytopathology 49, 135-156.
23. Denancé N, Sánchez-Vallet A, Goffner D, Molina A. 2013. Disease resistance or growth: The role of plant hormones in balancing immune responses and fitness costs. Frontiers in Plant Science, 4, 155.
24. Dhakshinamoorthy S, Mariama K, Elsen A, De Waele D. 2014. Phenols and lignin are involved in the defence response of banana (Musa) plants to Radopholus similis infection. Nematology 16, 565-576.
25. Dodds PN, Rathjen JP. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics 11, 539-548.
26. Doke N. 1983. Involvement of superoxide anion generation in the hypersensitive response of potato- Tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiological Plant Pathology 23, 345-357.
27. Enstone DE, Peterson CA, Ma FS. 2002. Root endodermis and exodermis: Structure, function, and responses to the environment. Journal of Plant Growth Regulation 21, 335-351.
28. Feng B, Shan L. 2014. ROS open roads to roundworm infection. Science Signaling 7, pe10.
29. Franke R, Schreiber L. 2007. Suberin- A biopolyester forming apoplastic plant interfaces. Current Opinion in Plant Biology 10, 252-259.
30. Goodridge HS, Marshall FA, Else KJ, Houston KM, Egan C, Al-Riyami L, Liew FY, Harnett W, Harnett MM. 2005. Immunomodulation via novel use of TLR4 by the filarial nematode phosphorylcholine-containing secreted product, ES-62. Journal of Immunology 174, 284-293.
31. Goverse A, Smant G. 2014. The activation and suppression of plant innate immunity by parasitic nematodes. Annual Review of Phytopathology 52, 243-265.
32. Glazebrook J, Chen WJ, Estes B, Chang HS, Nawrath C, Métraux JP, Zhu T, Katagiri F. 2003. Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. The Plant Journal, 34, 217-228.
33. Grundler FMW, Sobczak M, Lange S. 1997. Defence responses of Arabidopsis thaliana during invasion and feeding site induction by the plant-parasitic nematode Heterodera glycines. Physiological and Molecular Plant Pathology 50, 419-429.
34. Gutjahr C, Paszkowski U. 2009. Weights in the balance: jasmonic acid and salicylic acid signaling in root-biotroph interactions. Molecular Plant- Microbe Interactions 22, 763-772.
35. Hahn MG, Darvill AG, Albersheim P. 1981. Host-pathogen interactions. XVIV. The endogenous elicitor, a fragment of a plant-cell wall polysaccharide that elicits phytoalexin accumulation in soybeans. Plant Physiology 68, 1161-1169.
36. Heese A, Hann DR, Gimenez-Ibanez S, Jones AME, He K, Li J, Schroeder JI, Peck SC, Rathjen JP. 2007. The receptorlike kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences, USA 104, 12217-12222.
37. Hewezi T, Howe PT, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ. 2010. Arabidopsis spermidine synthase is targeted by an effector protein of the cyst nematode Heterodera schachtii. Plant Physiology 152, 968-984.
38. Hofmann J, Youssef-Banora M, de Almeida-Engler J, Grundler FMW. 2010. The role of callose deposition along plasmodesmata in nematode feeding sites. Molecular Plant-Microbe Interactions 23, 549-557.
39. Hsueh YP, Mahanti P, Schroeder FC, Sternberg PW. 2013. Nematode- Trapping fungi eavesdrop on nematode pheromones. Current Biology 23, 83-86.
40. Hussey RS, Grundler FMW. 1998. Nematode parasitism of plants. In: Perry RN, Wright J, eds. Physiology and biochemistry of free-living and plant parasitic nematodes . Oxford: CABI International Press, 213-243.
41. Hussey RS, Mims CW, Westcott SW. 1992. Immunocytochemical localization of callose in root cortical-cells parasitized by the ring nematode Criconemella xenoplax. Protoplasma 171, 1-6.
42. Jammes F, Lecomte P, Almeida-Engler J, Bitton F, Martin-Magniette ML, Renou JP, Abad P, Favery B. 2005. Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. The Plant Journal 44, 447-458.
43. Jaouannet M, Maglianao M, Arguel MJ, Gourges M, Evangelisti E, Abad P, Rosso MN. 2013. The root-knot nematode calreticulin Mi-CRT is a key effector in plant defense suppression. Molecular Plant-Microbe Interactions 26, 97-105.
44. Jaubert S, Laffaire JB, Abad P, Rosso MN. 2002. A polygalacturonase of animal origin isolated from the root-knot nematode Meloidogyne incognita. FEBS Letters 522, 109-112.
45. Ji H, Kyndt T, He W, Vanholme B, Gheysen G. 2015. β-Aminobutyric acid-induced resistance against root-knot nematodes in rice is based on increased basal defense. Molecular Plant-Microbe Interactions 28, 519-533.
46. Ji HL, Gheysen G, Denil S, et al. 2013. Transcriptional analysis through RNA sequencing of giant cells induced by Meloidogyne graminicola in rice roots. Journal of Experimental Botany 64, 3885-3898.
47. Jones JDG, Dangl JL. 2006. The plant immune system. Nature 444, 323-329.
48. Jones JT, Haegeman A, Danchin EGJ, et al. 2013. Top 10 plantparasitic nematodes in molecular plant pathology. Molecular Plant Pathology 14, 946-961.
49. Kadota Y, Sklenar J, Derbyshire P, et al. 2014. Direct regulation of the NADPH oxidase RBOHD by the PRR- Associated kinase BIK1 during plant immunity. Molecular Cell 54, 43-55.
50. Kammerhofer N, Radakovic Z, Regis MAJ, Dobrev P, Vankova R, Grundler FMW, Siddique S, Hofmann J, Wieczorek K. 2015. Role of stress-related hormones in plant defense during early infection of the cyst nematode Heterodera schachtii in Arabidopsis. New Phytologist 207, 778-789.
51. Kessler A, Baldwin IT. 2002. Plant responses to insect herbivory: The emerging molecular analysis. Annual Review of Plant Biology 53, 299-328.
52. Kyndt T, Denil S, Haegeman A, Trooskens G, Bauters L, Van Criekinge W, De Meyer T, Gheysen G. 2012. Transcriptional reprogramming by root knot and migratory nematode infection in rice. New Phytologist 196, 887-900.
53. Kyndt T, Fernandez D, Gheysen G. 2014. Plant-parasitic nematode infections in rice: Molecular and cellular insights. Annual Review of Phytopathology 52, 135-153.
54. Kyndt T, Vieira P, Gheysen G, de Almeida-Engler J. 2013. Nematode feeding sites: unique organs in plant roots. Planta 238, 807-818.
55. Lambert KN, Ferrie BJ, Nombela G, Brenner ED, Williamson VM. 1999. Identification of genes whose transcripts accumulate rapidly in tomato after root-knot nematode infection. Physiological and Molecular Plant Pathology 55, 341-348.
56. Lans H, Jansen G. 2007. Multiple sensory G proteins in the olfactory gustatory and nociceptive neurons modulate longevity in Caenorhabditis elegans. Developmental Biology 303, 474-482.
57. Levine A, Tenhaken R, Dixon R, Lamb C. 1994. H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79, 583-593.
58. Liu YQ, Wu H, Chen H, et al. 2015. A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nature Biotechnology 33, 301-305.
59. Lozano-Torres JL, Wilbers RHP, Warmerdam S, et al. 2014. Apoplastic venom allergen-like proteins of cyst nematodes modulate the activation of basal plant innate immunity by cell surface receptors. PLOS Pathogens 10, e1004569.
60. Ludewig AH, Schroeder FC. 2013. Ascaroside signaling in C. elegans. In: Kuwabara P, ed. WormBook. The C. elegans research community 18, 1-23.
61. Lulai EC, Corsini DL. 1998. Differential deposition of suberin phenolic and aliphatic domains and their roles in resistance to infection during potato tuber (Solanum tuberosum L.) wound-healing. Physiological and Molecular Plant Pathology 53, 209-222.
62. Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J. 2011. Callose deposition: A multifaceted plant defense response. Molecular Plant-Microbe Interactions 24, 183-193.
63. Macho AP, Zipfel C. 2014. Plant PRRs and the activation of innate immune signaling. Molecular Cell 54, 263-272.
64. Manosalva P, Manohar M, von Reuss SH, et al. 2015. Conserved nematode signalling molecules elicit plant defenses and pathogen resistance. Nature Communications 6, 7795.
65. Mantelin S, Thorpe P, Jones JT. 2015. Suppression of plant defences by plant-parasitic nematodes. In: Escobar C, Fenoll C, eds. Plant nematode interactions: A view on compatible interrelationships. Oxford: Academic Press, 325-334.
66. Martins I, Hartmann DO, Paula PC, et al. 2014. Elucidating how the saprophytic fungus Aspergillus nidulans uses the plant polyester suberin as carbon source. BMC Genomics 15, 1-19.
67. McClure MA, Bird AF. 1976. The tylenchid (Nematoda) egg-shell: formation of the egg-shell in Meloidogyne Javanica. Parasitology 72, 29-39.
68. Melillo MT, Leonetti P, Bongiovanni M, Castagnone-Sereno P, Bleve-Zacheo T. 2006. Modulation of reactive oxygen species activities and H2O2 accumulation during compatible and incompatible tomato-rootknot nematode interactions. New Phytologist 170, 501-512.
69. Monaghan J, Zipfel C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Current Opinion in Plant Biology 15, 349-357.
70. Montillet JL, Chamnongpol S, Rusterucci C, Dat J, van de Cotte B, Agnel JP, Battesti C, Inzé D, Van Breusegem F, Triantaphylides C. 2005. Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiology 138, 1516-1526.
71. Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N. 2012. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. Proceedings of the National Academy of Sciences, USA 109, 10101-10106.
72. Ofong AU, Pearce RB. 1994. Suberin degradation by Rosellinia desmazieresii. European Journal of Forest Pathology 24, 316-322.
73. Patel N, Hamamouch N, Li C, Hewezi T, Hussey RS, Baum TJ, Mitchum MG, Davis EL. 2010. A nematode effector protein similar to annexins in host plants. Journal of Experimental Botany 61, 235-248.
74. Peng HC, Kaloshian I. 2014. The tomato leucine-rich repeat receptor-like kinases SlSERK3A and SlSERK3B have overlapping functions in bacterial and nematode innate immunity. PLOS One 9, e93302.
75. Perrigoue JG, Marshall FA, Artis D. 2008. On the hunt for helminths: innate immune cells in the recognition and response to helminth parasites. Cellular Microbiology 10, 1757-1764.
76. Perry RN, Trett WM. 1986. Ultrastructure of the eggshell of Heterodera schachtii and H. glycines. Revue de Nematology 9, 399-403.
77. Pitcher RS, Patrick ZA, Mountain WB. 1960. Studies on the host- parasite relations of Pratylenchus penetrans (Cobb) to apple seedlings. Nematologica 5, 309-314.
78. Portillo M, Cabrera J, Lindsey K, et al. 2013. Distinct and conserved transcriptomic changes during nematode-induced giant cell development in tomato compared with Arabidopsis: A functional role for gene repression. New Phytologist 197, 1276-1290.
79. Quentin M, Abad P, Favery B. 2013. Plant parasitic nematode effectors target host defense and nuclear functions to establish feeding cells. Frontiers in Plant Science 4, 53.
80. Rai KM, Balasubramanian KV, Welker CM, Pang M, Hii MM, Mendu V. 2015. Genome wide comprehensive analysis and web resource development on cell wall degrading enzymes from phyto-parasitic nematodes. BMC Plant Biology 15, 187.
81. Ranathunge K, Schreiber L, Franke R. 2011. Suberin research in the genomics era-new interest for an old polymer. Plant Science 180, 399-413.
82. Rehman S, Postma W, Tytgat T, et al. 2009. A secreted SPRY domain-containing protein (SPRYSEC) from the plant-parasitic nematode Globodera rostochiensis interacts with a CC-NB-LRR orotein from a susceptible tomato. Molecular Plant-Microbe Interactions 22, 330-340.
83. Sasser JN, Freckman DW. 1986. A world perspective on nematology- The role of the society. Journal of Nematology 18, 596-597.
84. Schroeder FC. 2015. Modular assembly of primary metabolic building blocks: A chemical language in C. elegans. Chemistry & Biology 22, 7-16.
85. Schwessinger B, Roux M, Kadota Y, Ntoukakis V, Sklenar J, Jones A, Zipfel C. 2011. Phosphorylation-dependent differential regulation of plant growth, cell death, and innate immunity by the regulatory receptorlike kinase BAK1. PLOS Genetics 7, e1002046.
86. Shiu S, Bleecker AB. 2001. Plant receptor-like kinase gene family: diversity, function, and signaling. Science's STKE 113, re22.
87. Siddique S, Matera C, Radakovic ZS, Hasan MS, Gutbrod P, Rozanska E, Sobczak M, Torres MA, Grundler FMW. 2014. Parasitic worms stimulate host NADPH oxidases to produce reactive oxygen species that limit plant cell death and promote infection. Science Signaling 7, ra33.
88. Spiegel Y, McClure MA. 1995. The surface-coat of plant-parasitic nematodes: chemical composition, origin, and biological role- A review. Journal of Nematology 27, 127-134.
89. Szakasits D, Heinen P, Wieczorek K, Hofmann J, Wagner F, Kreil DP, Sykacek P, Grundler FMW, Bohlmann H. 2009. The transcriptome of syncytia induced by the cyst nematode Heterodera schachtii in Arabidopsis roots. The Plant Journal 57, 771-784.
90. Taddese B, Upton GJG, Bailey GR, Jordan SRD, Abdulla NY, Reeves PJ, Reynolds CA. 2014. Do plants contain G protein-coupled receptors? Plant Physiology 164, 287-307.
91. Torres MA, Dangl JL, Jones JDG. 2002. Arabidopsis gp91phox homologues AtrbohD and AtrbohF are required for accumulation of reactive oxygen intermediates in the plant defense response. Proceedings of the National Academy of Sciences, USA 99, 517-522.
92. Torres MA, Jones JDG, Dangl JL. 2005. Pathogen-induced, NADPH oxidase-derived reactive oxygen intermediates suppress spread of cell death in Arabidopsis thaliana. Nature Genetics 37, 1130-1134.
93. Torres MA, Jones JDG, Dangl JL. 2006. Reactive oxygen species signaling in response to pathogens. Plant Physiology 141, 373-378.
94. Umemoto N, Kakitani M, Iwamatsu A, Yoshikawas M, Yamaoka N, Ishida I. 1995. The structure and function of a soybean β-glucan-elicitorbinding protein. Proceedings of the National Academy of Sciences, USA 94, 1029-1034.
95. Underwood W. 2012. The plant cell wall: A dynamic barrier against pathogen invasion. Frontiers in Plant Science 3, 85.
96. Veronico P, Melillo MT, Saponaro C, Leonetti P, Picardi E, Jones JT. 2011. A polygalacturonase-inhibiting protein with a role in pea defence against the cyst nematode Heterodera goettingiana. Molecular Plant Pathology 12, 275-287.
97. von Reuss SH, Bose N, Srinivasan J, Yim JJ, Judkins JC, Sternberg PW, Schroeder FC. 2012. Comparative metabolomics reveals biogenesis of Ascarosides, a modular library of small-molecule signals in C. elegans. Journal of the American Chemical Society 134, 1817-1824.
98. Wan JR, Zhang XC, Neece D, Ramonell KM, Clough S, Kim SY, Stacey MG, Stacey G. 2008. A LysM receptor-like kinase plays a critical role in chitin signaling and fungal resistance in Arabidopsis. The Plant Cell 20, 471-481.
99. Waetzig GH, Sobczak M, Grundler FMW. 1999. Localization of hydrogen peroxide during the defence response of Arabidopsis thaliana against the plant-parasitic nematode Heterodera glycines. Nematology 1, 681-686.
100. Wieczoreck K. 2015. Cell wall alterations in nematode infected roots. In: Escobar C, Fenoll C, eds. Plant nematode interactions- A view on compatible interrelationships, Vol. 73. Dordrecht, The Netherland: Springer, 61-90.
101. Wolf S, Deom CM, Beachy R, Lucas WJ. 1991. Plasmodesmatal function is probed using transgenic tobacco plants that express a virus movement protein. The Plant Cell 3, 593-604.
102. Wuyts N, Lognay G, Swennen R, De Waele D. 2006. Nematode infection and reproduction in transgenic and mutant Arabidopsis and tobacco with an altered phenylpropanoid metabolism. Journal of Experimental Botany 57, 2825-2835.
103. Wuyts N, Lognay G, Verscheure M, Marlier M, De Waele D, Swennen R. 2007. Potential physical and chemical barriers to infection by the burrowing nematode Radopholus similis in roots of susceptible and resistant banana (Musa spp.). Plant Pathology 56, 878-890.
104. Wyss U, Zunke U. 1986. Observations on the behavior of second stage juveniles of Heterodera schachtii inside host roots. Revue de Nématologie 9, 153-165.
105. Wyss U, Grundler FMW, Munch A. 1992. The parasitic behaviour of second-stage juveniles of Meloidogyne incognita in roots of Arabidopsis thaliana. Nematologica 38, 98-111.
106. Yoshioka H, Numata N, Nakajima K, Katou S, Kawakita K, Rowland O, Jones JDG, Doke N. 2003. Nicotiana benthamiana gp91phox homologs NbrbohA and NbrbohB participate in H2O2 accumulation and resistance to Phytophthora infestans. The Plant Cell 15, 706-718.
107. Zacheo G, Bleve-Zacheo T, Lamberti F. 1982. Role of peroxidase and superoxide dismutase activity in resistant and susceptible tomato cultivars infested by Meloidogyne incognita. Nematologia Mediterranea 10, 75-80.
108. Zeier J, Goll A, Yokoyama M, Karahara I, Schreiber L. 1999. Structure and chemical composition of endodermal and rhizodermal hypodermal walls of several species. Plant, Cell and Environment 22, 271-279.
109. Zwaal RR, Mendel JE, Sternberg PW, Plasterk RHA. 1997. Two neuronal G proteins are involved in chemosensation of the Caenorhabditis elegans Dauer-inducing pheromone. Genetics 145, 715-727.