- Email: [email protected]
In This Issue “The First Touch”
Physiological and Molecular Plant Pathology (2000) 56, 49–50 doi : 10.1006\pmpp.2000.0257, available online at http :\\www.idealibrary.com on
In This Issue ‘‘ The First Touch ’’ MICHE' LE C. H E A TH The early recognition events that take place between plant and microbe in both pathogenic and mutualistic associations have been the subject of much interest and investigation. Yet the subtlety and complexity of these events are still only just beginning to be revealed. It has long been recognized that soil micro-organisms may respond to secretory products from their potential host plants prior to any physical contact [13] and in this issue, Bagga and Straney [1] report that macroconidia of the fungus, Nectria haematococca, germinate in response to the same flavonoids that induce nod gene expression in peaspecific rhizobia. As for many examples of fungal morphogenesis, including infection structure formation [7, 9], cAMP appears to be involved in the response and Bagga and Straney [1] provide a basis for the rise in cAMP levels by suggesting that plant flavonoids may prevent cAMP degradation by inhibiting cAMP phosphodiesterase. Pre-contact communication is only part of the recognition story, however, and although zoospores and hyphal germlings of the oomycete, Phytophthora sojae, can chemotropically respond to host isoflavones, tactile responses of hyphae may be more important determinants of hyphal growth once the pathogen touches the root [13]. The role of plant surface topography in directing fungal germ tube growth and the differentiation of infection structures has been well documented, particularly for rust fungi [16]. In one of the best demonstrations of this phenomenon, Wynn [18] showed that the bean rust fungus could locate and form appressoria on stomata of plastic replicas of the leaf surface. Although the responsive region of the germ tube has been demonstrated to be that part in contact with the substratum near the hyphal apex [5], how this topography is transduced into signals within the fungus is still not fully understood. However, the fact that contact-stimulated appressorium formation can be inhibited by Arg-Gly-Asp (RGD)-containing peptides suggests a role for integrin-like proteins that, like integrins in mammals, mediate interactions between extracellular materials and the cytoskeleton [6]. Nevertheless, contact stimulus may not be the only trigger of differentiation in other rust fungi, as host topography alone is not sufficient to explain the high efficiency of appressorium induction seen in io in some cereal rust fungi [4]. Chemical, rather than physical, cues seem to be particularly important in the recognition of host surfaces by the rice blast fungus, Magnaporthe grisea. Conidia carry lipophilic self-inhibitors of germination, the action of 0885–5765\00\020049j02 $35.00\0
which can be relieved by plant surface wax when they land of the plant surface [10]. In addition, there is evidence [2] that a fungal hydrophobin, coded by gene MPG1, is involved in the interaction with, and recognition of, the host surface and that the ability of this protein to self-assemble may have been co-opted into serving a role in surface perception and appressorium formation [17]. A number of plant cues may be involved in the latter process, however, as it can be induced in attached germ tubes by specific cutin monomers and lipids in nanomolar quantities ; cutinase secretion by the fungus may cause release of appropriate cutin monomers to facilitate surface attachment and recognition [8]. A similar involvement of multiple plant cues in early fungal responses to host surfaces has been demonstrated for spore germination and appressorium formation by Colletotrichum gloeosporioides. These processes are induced specifically by surface wax from the avocado host, and can be inhibited by waxes of nonhost species. They also can be induced by ethylene via a different receptor, although both stimuli cause the phosphorylation of the same set of proteins [12]. Conidia of the barley mildew fungus, Blumeria graminis f. sp. hordei release extracellular matrix material within seconds after touching a suitable hydrophobic surface [3]. However, they have been considered to be unable to take up compounds from the plant prior to germination. In this issue, Nielsen et al. [15] demonstrate not only that they can take up anionic low-molecular-weight compounds from surfaces that induce the release of extracellular matrix, but that they do so most rapidly (within 30 min) from the surface of the host plant. They suggest that this facilitated transport could be a mechanism for the recognition of the host, and that this recognition determines the site and direction of germ tube emergence from the conidium and affects later stages of infection structure formation. This variety of interactions with the plant surface indicate that many, if not most, pathogenic fungi are adapted to respond to subtle, and probably multiple, cues from the surfaces of their hosts, often at the ‘‘ first touch ’’. Data also is accumulating that the plant response may be almost as rapid. Plant epidermal cells, for example, respond to directly-penetrating biotrophic pathogenic fungi, just after [14] or even before [11] the fungus begins to penetrate the plant wall, and long before it enters the cell lumen. In total, the evidence is strong that plantfungal interactions begin, and perhaps their outcomes are # 2000 Academic Press
50
M. C. Heath
determined, during the very first minutes of association for foliar pathogens and perhaps even earlier for fungi in the soil. REFERENCES 1. Bagga S, Straney D. 2000. Modulation of cAMP and phosphodiesterase activity by flavonoids which induce spore germination of Nectria haematococca MP VI (Fusarium solani). Physiological and Molecular Plant Pathology 56 : 51–61. 2. Beckerman JL, Ebbole DJ. 1996. MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Molecular Plant-Microbe Interactions 9 : 450–456. 3. Carver TLW, Kunoh H, Thomas BJ, Nicholson RL. 1999. Release and visualization of the extracellular matrix of conidia of Blumeria graminis. Mycological Research 103 : 547–560. 4. Collins TJ, Read ND. 1997. Appressorium induction by topographical signals in six cereal rusts. Physiological and Molecular Plant Pathology 51 : 169–179. 5. Corre# a A Jr, Hoch, HC. 1995. Identification of thigmoresponsive loci for cell differentiation in Uromyces germlings. Protoplasma 186 : 34–40. 6. Corre# a JA, Staples RC, Hoch HC. 1996. Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194 : 91–102. 7. Dean RA. 1997. Signal pathways and appressorium morphogenesis. Annual Reiew of Phytopathology. 35 : 211–34. 8. Gilbert, RD, Johnson AM, Dean RA. 1996. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiological and Molecular Plant Pathology 48 : 335–346. 9. Hall AA, Gurr SJ. 2000. Initiation of appressorial germ tube differentiation in appressorial hooking : distinct morphological events regulated by cAMP signalling in Blumeria graminis f. sp. hordei. Physiological and Molecular Plant Pathology 56 : 39–46.
10. Hegde Y, Kolattukudy PE. 1997. Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea. Physiological and Molecular Plant Pathology 51 : 75–84. 11. Kobayashi I, Kobayashi Y, Yamaoka N, Kunoh H. 1992. Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Responses of microtubules and actin filaments in barley coleoptile cells to penetration attempts. Canadian Journal of Botany 70 : 1815–1823. 12. Kolattukudy PE, Rogers LM, Li D, Hwang C-S, Flaishman MA. 1995. Surface signaling in pathogenesis. Proceedings of the National Academy of Sciences USA 92 : 4080–4087. 13. Morris PF, Bone E, Tyler BM. 1998. Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiology 117 : 1171–1178. 14. Mould MJR, Heath MC. 1999. Ultrastructural evidence of differential changes in transcription, translation, and cortical microtubules during in planta penetration of cells resistant of susceptible to rust infection. Physiological and Molecular Plant Pathology 55 : 225–236. 15. Nielsen KA, Nicholson RL, Carver TLW, Kunoh H, Oliver RP. 2000. First touch : An immediate response to surface recognition in conidia of Blumeria graminis. Physiological and Molecular Plant Pathology 56 : 63–70. 16. Read ND, Kellock LJ, Knight H, Trewavas AJ. 1992. Contact sensing during infection by fungal pathogens. In : Callow JA, Green JR, eds. Perspecties in Plant Cell Recognition. Society for Experimental Biology Seminar Series 48, Cambridge : Cambridge University Press, pp. 137–172. 17. Talbot NJ, Kershaw MJ, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE. 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8 : 985–999. 18. Wynn WK. 1976. Appressorium formation over stomates by the beam rust fungus : response to a surface contact stimulus. Phytopathology 66 : 136–146.
In This Issue ‘‘ The First Touch ’’ MICHE' LE C. H E A TH The early recognition events that take place between plant and microbe in both pathogenic and mutualistic associations have been the subject of much interest and investigation. Yet the subtlety and complexity of these events are still only just beginning to be revealed. It has long been recognized that soil micro-organisms may respond to secretory products from their potential host plants prior to any physical contact [13] and in this issue, Bagga and Straney [1] report that macroconidia of the fungus, Nectria haematococca, germinate in response to the same flavonoids that induce nod gene expression in peaspecific rhizobia. As for many examples of fungal morphogenesis, including infection structure formation [7, 9], cAMP appears to be involved in the response and Bagga and Straney [1] provide a basis for the rise in cAMP levels by suggesting that plant flavonoids may prevent cAMP degradation by inhibiting cAMP phosphodiesterase. Pre-contact communication is only part of the recognition story, however, and although zoospores and hyphal germlings of the oomycete, Phytophthora sojae, can chemotropically respond to host isoflavones, tactile responses of hyphae may be more important determinants of hyphal growth once the pathogen touches the root [13]. The role of plant surface topography in directing fungal germ tube growth and the differentiation of infection structures has been well documented, particularly for rust fungi [16]. In one of the best demonstrations of this phenomenon, Wynn [18] showed that the bean rust fungus could locate and form appressoria on stomata of plastic replicas of the leaf surface. Although the responsive region of the germ tube has been demonstrated to be that part in contact with the substratum near the hyphal apex [5], how this topography is transduced into signals within the fungus is still not fully understood. However, the fact that contact-stimulated appressorium formation can be inhibited by Arg-Gly-Asp (RGD)-containing peptides suggests a role for integrin-like proteins that, like integrins in mammals, mediate interactions between extracellular materials and the cytoskeleton [6]. Nevertheless, contact stimulus may not be the only trigger of differentiation in other rust fungi, as host topography alone is not sufficient to explain the high efficiency of appressorium induction seen in io in some cereal rust fungi [4]. Chemical, rather than physical, cues seem to be particularly important in the recognition of host surfaces by the rice blast fungus, Magnaporthe grisea. Conidia carry lipophilic self-inhibitors of germination, the action of 0885–5765\00\020049j02 $35.00\0
which can be relieved by plant surface wax when they land of the plant surface [10]. In addition, there is evidence [2] that a fungal hydrophobin, coded by gene MPG1, is involved in the interaction with, and recognition of, the host surface and that the ability of this protein to self-assemble may have been co-opted into serving a role in surface perception and appressorium formation [17]. A number of plant cues may be involved in the latter process, however, as it can be induced in attached germ tubes by specific cutin monomers and lipids in nanomolar quantities ; cutinase secretion by the fungus may cause release of appropriate cutin monomers to facilitate surface attachment and recognition [8]. A similar involvement of multiple plant cues in early fungal responses to host surfaces has been demonstrated for spore germination and appressorium formation by Colletotrichum gloeosporioides. These processes are induced specifically by surface wax from the avocado host, and can be inhibited by waxes of nonhost species. They also can be induced by ethylene via a different receptor, although both stimuli cause the phosphorylation of the same set of proteins [12]. Conidia of the barley mildew fungus, Blumeria graminis f. sp. hordei release extracellular matrix material within seconds after touching a suitable hydrophobic surface [3]. However, they have been considered to be unable to take up compounds from the plant prior to germination. In this issue, Nielsen et al. [15] demonstrate not only that they can take up anionic low-molecular-weight compounds from surfaces that induce the release of extracellular matrix, but that they do so most rapidly (within 30 min) from the surface of the host plant. They suggest that this facilitated transport could be a mechanism for the recognition of the host, and that this recognition determines the site and direction of germ tube emergence from the conidium and affects later stages of infection structure formation. This variety of interactions with the plant surface indicate that many, if not most, pathogenic fungi are adapted to respond to subtle, and probably multiple, cues from the surfaces of their hosts, often at the ‘‘ first touch ’’. Data also is accumulating that the plant response may be almost as rapid. Plant epidermal cells, for example, respond to directly-penetrating biotrophic pathogenic fungi, just after [14] or even before [11] the fungus begins to penetrate the plant wall, and long before it enters the cell lumen. In total, the evidence is strong that plantfungal interactions begin, and perhaps their outcomes are # 2000 Academic Press
50
M. C. Heath
determined, during the very first minutes of association for foliar pathogens and perhaps even earlier for fungi in the soil. REFERENCES 1. Bagga S, Straney D. 2000. Modulation of cAMP and phosphodiesterase activity by flavonoids which induce spore germination of Nectria haematococca MP VI (Fusarium solani). Physiological and Molecular Plant Pathology 56 : 51–61. 2. Beckerman JL, Ebbole DJ. 1996. MPG1, a gene encoding a fungal hydrophobin of Magnaporthe grisea, is involved in surface recognition. Molecular Plant-Microbe Interactions 9 : 450–456. 3. Carver TLW, Kunoh H, Thomas BJ, Nicholson RL. 1999. Release and visualization of the extracellular matrix of conidia of Blumeria graminis. Mycological Research 103 : 547–560. 4. Collins TJ, Read ND. 1997. Appressorium induction by topographical signals in six cereal rusts. Physiological and Molecular Plant Pathology 51 : 169–179. 5. Corre# a A Jr, Hoch, HC. 1995. Identification of thigmoresponsive loci for cell differentiation in Uromyces germlings. Protoplasma 186 : 34–40. 6. Corre# a JA, Staples RC, Hoch HC. 1996. Inhibition of thigmostimulated cell differentiation with RGD-peptides in Uromyces germlings. Protoplasma 194 : 91–102. 7. Dean RA. 1997. Signal pathways and appressorium morphogenesis. Annual Reiew of Phytopathology. 35 : 211–34. 8. Gilbert, RD, Johnson AM, Dean RA. 1996. Chemical signals responsible for appressorium formation in the rice blast fungus Magnaporthe grisea. Physiological and Molecular Plant Pathology 48 : 335–346. 9. Hall AA, Gurr SJ. 2000. Initiation of appressorial germ tube differentiation in appressorial hooking : distinct morphological events regulated by cAMP signalling in Blumeria graminis f. sp. hordei. Physiological and Molecular Plant Pathology 56 : 39–46.
10. Hegde Y, Kolattukudy PE. 1997. Cuticular waxes relieve self-inhibition of germination and appressorium formation by the conidia of Magnaporthe grisea. Physiological and Molecular Plant Pathology 51 : 75–84. 11. Kobayashi I, Kobayashi Y, Yamaoka N, Kunoh H. 1992. Recognition of a pathogen and a nonpathogen by barley coleoptile cells. III. Responses of microtubules and actin filaments in barley coleoptile cells to penetration attempts. Canadian Journal of Botany 70 : 1815–1823. 12. Kolattukudy PE, Rogers LM, Li D, Hwang C-S, Flaishman MA. 1995. Surface signaling in pathogenesis. Proceedings of the National Academy of Sciences USA 92 : 4080–4087. 13. Morris PF, Bone E, Tyler BM. 1998. Chemotropic and contact responses of Phytophthora sojae hyphae to soybean isoflavonoids and artificial substrates. Plant Physiology 117 : 1171–1178. 14. Mould MJR, Heath MC. 1999. Ultrastructural evidence of differential changes in transcription, translation, and cortical microtubules during in planta penetration of cells resistant of susceptible to rust infection. Physiological and Molecular Plant Pathology 55 : 225–236. 15. Nielsen KA, Nicholson RL, Carver TLW, Kunoh H, Oliver RP. 2000. First touch : An immediate response to surface recognition in conidia of Blumeria graminis. Physiological and Molecular Plant Pathology 56 : 63–70. 16. Read ND, Kellock LJ, Knight H, Trewavas AJ. 1992. Contact sensing during infection by fungal pathogens. In : Callow JA, Green JR, eds. Perspecties in Plant Cell Recognition. Society for Experimental Biology Seminar Series 48, Cambridge : Cambridge University Press, pp. 137–172. 17. Talbot NJ, Kershaw MJ, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE. 1996. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 8 : 985–999. 18. Wynn WK. 1976. Appressorium formation over stomates by the beam rust fungus : response to a surface contact stimulus. Phytopathology 66 : 136–146.