Skip to main content Accessibility help
×
Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-24T15:18:47.246Z Has data issue: false hasContentIssue false

3 - Environmental sensing and the filamentous fungal lifestyle

from I - Imaging and modelling of fungi in the environment

Published online by Cambridge University Press:  03 November 2009

Nick D. Read
Affiliation:
Institute of Cell Biology, University of Edinburgh
Geoffrey Gadd
Affiliation:
University of Dundee
Sarah C. Watkinson
Affiliation:
University of Oxford
Paul S. Dyer
Affiliation:
University of Nottingham
Get access

Summary

Introduction

The majority of fungi have a filamentous lifestyle. The evolution of the hypha has been pivotal to the success of filamentous fungi and in determining the uniqueness of their lifestyle. It has also had important consequences in determining the modes of morphogenesis of filamentous fungi, and how they operate as non-motile, heterotrophic organisms (Read, 1994). This review focuses on hyphal and colony morphogenesis and how it is influenced by environmental signals in the context of the filamentous fungal lifestyle.

The supracellular, cellular and multicellular nature of filamentous fungi

The defining cellular element of the filamentous fungi is the hypha (Figs. 3.1–3.6). Hyphae possess a unique combination of structural, behavioural and functional attributes that clearly distinguish them from uninucleate animal and plant cells. The vegetative hypha is a tip-growing cellular element (Harris et al., 2005) (Figs. 3.1, 3.2) that undergoes regular branching (Trinci, 1983; Turner & Harris, 1997) (Figs. 3.3, 3.4), is typically multinucleate (Fig. 3.3) (Freitag et al., 2004), and possesses incomplete cross-walls (septa) which, when open, allow movement of cytoplasm and organelles between hyphal compartments (Harris, 2001) (Fig. 3.2). In sub-peripheral regions of the colony, hyphae frequently fuse with one another (Read & Roca, 2006) (Fig. 3.3) and septal pores often become blocked (Gull, 1978) (Fig. 3.2). Vegetative hyphae thus have a supracellular nature because they are part of a network of interconnected hyphal compartments and hyphae within the colony (Fig. 3.1).

Type
Chapter
Information
Publisher: Cambridge University Press
Print publication year: 2007

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alex, L. A., Borkovich, K. A. & Simon, M. I. (1996). Hyphal development in Neurospora crassa: involvement of a two-component histidine kinase. Proceedings of the National Academy of Sciences of the USA 93, 3416–21.CrossRefGoogle ScholarPubMed
Baasiri, R. A., Lu, X., Rowley, P. S., Turner, G. E. & Borkovich, K. A. (1997). Overlapping functions for two G protein α subunits in Neurospora crassa. Genetics 147, 137–45.Google ScholarPubMed
Banno, S., Ochiai, N., Noguchi, R., Kimura, M., Yamaguchi, I., Kanzaki, S., Murayama, T. & Fujimura, M. (2005). A catalytic subunit of cyclic AMP-dependent protein kinase, PKAC-1, regulates asexual differentiation in Neurospora crassa. Genes and Genetic Systems 80, 23–34.CrossRefGoogle ScholarPubMed
Bartnicki-Garcia, S. (2002). Hyphal tip growth: outstanding questions. In Molecular Biology of Fungal Development, ed. Osiewacz, H. D., pp. 29–58. New York: Marcel Dekker.CrossRefGoogle Scholar
Bartnicki-Garcia, S., Hergert, F. & Gierz, G. (1989). Computer simulation of fungal morphogenesis and the mathematical basis for hyphal tip growth. Protoplasma 153, 46–57.CrossRefGoogle Scholar
Beckett, A. (1981). The ultrastructure of septal pores and associated structures in the ascogenous hyphae and asci of Sordaria humana. Protoplasma 107, 127–47.CrossRefGoogle Scholar
Berridge, M. J., Bootman, M. D. & Roderick, H. L. (2003). Calcium signaling: dynamics, homeostasis and remodeling. Nature Reviews in Molecular and Cell Biology 4, 517–29.CrossRefGoogle Scholar
Bistis, G. N., Perkins, D. D. & Read, N. D. (2003). Different cell types in Neurospora crassa. Fungal Genetics Newsletter 50, 17–19.CrossRefGoogle Scholar
Bobrowicz, P., Pawlak, R., Correa, A., Bell-Pedersen, D. & Ebbole, D. J. (2002). The Neurospora crassa pheromone precursor genes are regulated by the mating type locus and the circadian clock. Molecular Microbiology 45, 795–804.CrossRefGoogle ScholarPubMed
Bobrowicz, P., Wilkinson, H. H. & Ebbole, D. J. (2005). A mitogen-activated protein kinase pathway essential for mating and contributing to vegetative growth in Neurospora crassa. Genetics 170, 1091–104.Google Scholar
Borkovich, K. A., Alex, L. A., Yarden, O., Freitag, M., Turner, G. E., Read, N. D., Seiler, S., Bell-Pederson, D., Paietta, J., Plesofskz, N., Plamann, M., Schulte, U., Mannhaupt, G., Nargang, F., Radford, A., Selitrennikoff, C., Galagan, J. E., Dunlap, J. C., Loros, J., Catcheside, D., Inoue, H., Aramazo, R., Polzmenis, M., Selker, E. U., Sachs, M. S., Marzluf, G. A., Paulsen, I., Davis, R., Ebbole, D. J., Yelter, A., Kalkman, E., O'Rourke, R., Bowring, F., Zeadon, J., Ishii, C., Suzuki, K., Sakai, W. & Pratt, R. (2004). Lessons from the genome sequence of Neurospora crassa: tracing the path from genomic blueprint to multicellular organism. Microbiological and Molecular Biology Reviews 68, 1–108.CrossRefGoogle ScholarPubMed
Bottone, E. J., Nagarsheth, N. & Chiu, K. (1998). Evidence of self-inhibition by filamentous fungi accounts for unidirectional hyphal growth in colonies. Canadian Journal of Microbiology 44, 390–3.CrossRefGoogle ScholarPubMed
Bracker, C. E., Murphy, D. J. & Lopez-Franco, R. (1997). Laser beam micromanipulation of cell morphogenesis in growing fungal hyphae. In Functional Imaging of Optical Manipulation of Living cells. Proceedings of SPIE, vol. 2983, ed. Farkas, D. L. & Tromberg, B. J., pp. 67–80. Bellingham, Washington, USA: International Society of Optical Engineering.Google Scholar
Bruno, K. S., Aramayo, R., Minke, P. F., Metzenberg, R. L. & Plamann, M. (1996). Loss of growth polarity and mislocalization of septa in a Neurospora mutant altered in the regulatory subunit of cAMP-dependent protein kinase. EMBO Journal 15, 5772–82.Google Scholar
Buller, A. H. R. (1931). Researches on Fungi, vol. 4. London: Longman.Google Scholar
Burow, G. B., Nesbitt, J., Dunlap, J. & Keller, N. P. (1997). Seed lipoxygenase products modulate Aspergillus mycotoxin biosynthesis. Molecular Plant-Microbe Interactions 10, 380–7.CrossRefGoogle Scholar
Chen, H., Fujita, M., Feng, Q., Clardy, J. & Fink, G. R. (2004). Tyrosol is a quorum-sensing molecule in Candida albicans. Proceedings of the National Academy of Sciences of the USA 101, 5048–52.CrossRefGoogle ScholarPubMed
Cooke, R. C. & Whipps, J. M. (1993). Ecophysiology of Fungi. London: Blackwell Scientific Publications.Google Scholar
Dean, R. A., Talbot, N. J., Ebbole, D. J., Farman, M. L., Mitchell, T. K., Orbach, M. J., Thon, M., Kulkarni, R., Xu, J. R., Pan, H., Read, N. D., Lee, Y. H., Carbone, I., Brown, D., Oh, Y. Y., Donofrio, N., Jeong, J. S., Soanes, D. M., Djonovic, S., Kolomiets, E., Rehmeyer, C., Li, W., Harding, M., Kim, S., Lebrun, M. H., Bohnert, H., Coughlan, S., Butler, J., Calvo, S., Ma, L. J., Nicol, R., Purcell, S., Nusbaum, C., Galagan, J. E. & Birren, B. W. (2005). The genome sequence of the rice blast fungus Magnaporthe grisea. Nature 434, 980–6.CrossRefGoogle ScholarPubMed
Dijksterhuis, J. (2003). Confocal microscopy of Spitzenkörper dynamics during growth and differentiation of rust fungi. Protoplasma 222, 53–9.CrossRefGoogle ScholarPubMed
d'Enfert, C., Bonini, B. M., Zapella, P. D., Fontaine, T., da Silva, A. M. & Terenzi, H. F. (1999). Neutral trehalases catalyse intracellular trehalose breakdown in the filamentous fungi Aspergillus nidulans and Neurospora crassa. Molecular Microbiology 32, 471–83.CrossRefGoogle ScholarPubMed
Enjalbert, B. & Whiteway, M. (2005). Release from quorum-sensing molecules triggers hyphal formation during Candida albicans resumption of growth. Eukaryotic Cell 4, 1203–10.CrossRefGoogle Scholar
Freitag, M., Hickey, P. C., Raju, N. B., Selker, E. U. & Read, N. D. (2004). GFP as a tool to analyze the organization, dynamics and function of nuclei and microtubules in Neurospora crassa. Fungal Genetics and Biology 41, 897–910.CrossRefGoogle ScholarPubMed
French, F. C. (1985). The bioregulatory action of flavor compounds on fungal spores and other propagules. Annual Review of Phytopathology 23, 173–99.CrossRefGoogle Scholar
Galagan, J., Calvo, S., Borkovich, K., Selker, E., Read, N. D., FitzHugh, W., Ma, L. P.-J., Smirnov, S., Purcell, S., Rehman, B., Elkins, T., Engels, R., Wang, S., Nielsen, C. B., Butler, J., Jaffe, D., Endrizzi, M., Qui, D., Planakiev, P., Bell-Pedersen, D., Nelson, M. A., Werner-Washburne, M., Selitrennikoff, C. P., Kinsey, J. A., Braun, E. L., Zelter, A., Schulte, U., Kothe, G. O., Jedd, G., Mewes, W., Staben, C., Marcotte, E., Greenberg, D., Roy, A., Foley, K., Naylor, J., Stange-Thomann, N., Barrett, R., Gnerre, S., Kamal, M., Kamvysselis, M., Bielke, C., Rudd, S., Frishman, D., Krystofova, S., Rasmussen, C., Metzenberg, R. L., Perkins, D. D., Kroken, S., Catcheside, D., Li, W., Pratt, R. J., Osmani, S. A., DeSouza, C. P. C., Glass, L., Orbach, M. J., Berglund, J. A., Voelker, R., Yarden, O., Plamann, M., Seiler, S., Dunlap, J., Radford, A., Amraayo, R., Natvig, D. O., Alex, L. A., Mannhaupt, G., Ebbole, D. J., Freitag, M., Paulsen, I., Sachs, M. S., Lander, E. S., Nusbaum, C., Birren, B. (2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859–68.CrossRefGoogle ScholarPubMed
Girbardt, M. (1957). Der Spitzenkörper von Polystictus versicolor. Planta 50, 47–59.CrossRefGoogle Scholar
Gooday, G. W. (1994). Hormones in mycelial fungi. In The Mycota, vol. 1, Growth, Differentiation and Sexuality, 1st edn, ed. Wessels, J. G. H. & Meinhardt, F., pp. 401–11. Berlin: Springer-Verlag.Google Scholar
Gow, N. A. R. (2004). New angles in mycology: studies in directional growth and directional motility. Mycological Research 108, 5–13.CrossRefGoogle ScholarPubMed
Gull, K. (1978). Form and function of septa in filamentous fungi. In The Filamentous Fungi, vol. 3, Developmental Mycology, ed. Smith, J. E. & Berry, D. R., pp. 78–93. London: Edward Arnold.Google Scholar
Harris, S. D. (2001). Septum formation in Aspergillus nidulans. Current Opinion in Microbiology 4, 736–9.CrossRefGoogle ScholarPubMed
Harris, S. D., Read, N. D., Roberson, R. W., Shaw, B., Seiler, S., Plamann, M. & Momany, M. (2005). Polarisome meets Spitzenkörper: microscopy, genetics, and genomics converge. Eukaryotic Cell 4, 225–9.CrossRefGoogle ScholarPubMed
Hickey, P. C., Jacobson, D., Read, N. D. & Glass, N. L. (2002). Live-cell imaging of vegetative hyphal fusion in Neurospora crassa. Fungal Genetics and Biology 37, 109–19.CrossRefGoogle ScholarPubMed
Hickey, P. C., Swift, S. R., Roca, M. G. & Read, N. D. (2005). Live-cell imaging of filamentous fungi using vital fluorescent dyes and confocal microscopy. In Methods in Microbiology, vol. 34, Microbial Imaging, ed. Savidge, T. & Pothoulakis, C., pp. 63–87. Amsterdam: Elsevier.Google Scholar
Hornby, J. M., Jensen, E. C., Lisec, A. D., Tasto, J. J., Jahnke, B., Shoemaker, R., Dussault, P. & Nickerson, K. W. (2004). Quorum sensing in the dimorphic fungus Candida albicans is mediated by farnesol. Applied and Environmental Microbiology 67, 2982–92.CrossRefGoogle Scholar
Ingold, C. T. (1971). Fungal Spores, their Liberation and Dispersal. Oxford: Clarendon Press.Google Scholar
Ivey, F. D., Hodge, P. N., Tunrer, G. E. & Borkovich, K. A. (1996). The Gαi homologue gna-1 controls multiple differentiation pathways in Neurospora crassa. Molecular Biology of the Cell 7, 1283–97.CrossRefGoogle Scholar
Ivey, F. D.Kays, A. M. & Borkovich, K. A. (2002). Shared and independent roles for a Gα protein and adenylyl cyclase in regulating development and stress responses in Neurospora crassa. Eukaryotic Cell 1, 634–42.CrossRefGoogle ScholarPubMed
Kana-Uchi, A., Yamashiro, C. T., Tanabe, S. & Murayama, T. (1997). A ras homologue of Neurospora crassa regulates morphology. Molecular and General Genetics 254, 427–32.Google ScholarPubMed
Kays, A. M. & Borkovich, K. A. (2005). Signal transduction pathways mediated by heterotrimeric G proteins. In The Mycota, vol. 3, Biochemistry and Molecular Biology, 2nd edn., ed. Brambl, R. & Marzluf, G. A., pp. 175–207. Berlin: Springer-Verlag.Google Scholar
Kays, A. M., Rowley, P. S., Baasiri, R. A. & Borkovich, K. A. (2000). Regulation of conidiation and adenylyl cyclase levels by the protein GNA-3 in Neurospora crassa. Molecular Cell Biology 20, 7693–705.CrossRefGoogle ScholarPubMed
Kim, H., Metzenberg, R. L. & Nelson, M. A. (2002). Multiple functions of mfa-1, a putative pheromone precursor gene of Neurospora crassa. Eukaryotic Cell 1, 987–99.CrossRefGoogle ScholarPubMed
Kruppa, M., Krom, B. P., Chauhan, N., Bambach, A. V., Cihlar, R. L. & Calderone, R. A. (2004). The two-component signal transduction protein Chk1p regulates quorum sensing in Candida albicans. Eukaryotic Cell 3, 1062–5.CrossRefGoogle ScholarPubMed
Krystofova, S. & Borkovich, K. A. (2005). The heterotrimeric G-protein subunits GNG-1 and GNB-1 form a Gβγ dimer required for normal female fertility, asexual development, and Gα protein levels in Neurospora crassa. Eukaryotic Cell 4, 365–78.CrossRefGoogle Scholar
Kulkarni, R. D., Thon, M. R., Pan, H. & Dean, R. A. (2005). Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biology 6, R24.CrossRefGoogle ScholarPubMed
Levin, D. E. (2005). Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiological and Molecular Biology Reviews 69, 292–305.Google ScholarPubMed
Lopez-Franco, R. & Bracker, C. E. (1996). Diversity and dynamics of the Spitzenkörper in growing hyphal tips of higher fungi. Protoplasma 195, 90–111.CrossRefGoogle Scholar
Lu, H. & McLaughlin, D. J. (2005). Ultrastructure of the septal pore apparatus and early septum initiation in Auricularia auricula-judae. Mycologia 83, 322–34.CrossRefGoogle Scholar
Lucas, J. A. (2004). Survival, surfaces and susceptibility – the sensory biology of pathogens. Plant Pathology 53, 679–91.CrossRefGoogle Scholar
Macko, V. & Staples, R. C. (1973). Regulation of uredospore germination and germ tube development. Bulletin of the Torrey Botanical Club 100, 223–9.CrossRefGoogle Scholar
Martin, S. W., Douglas, L. M. & Konopka, J. B. (2005). Cell cycle dynamics and quorum sensing in Candida albicans chlamydospores are distinct from budding and hyphal growth. Eukaryotic Cell 4, 1191–202.CrossRefGoogle ScholarPubMed
Neer, E. J. (1995). Heterotrimeric G proteins: organizers of transmembrane signals. Cell 80, 249–57.CrossRefGoogle ScholarPubMed
Pandey, A., Roca, G., Read, N. D. & Glass, N. L. (2004). Role of a MAP kinase pathway during conidial germination and hyphal fusion in Neurospora crassa. Eukaryotic Cell 3, 348–58.CrossRefGoogle ScholarPubMed
Prokisch, H., Yarden, O., Dieminger, M., Tropschug, M. & Barthelmess, I. B. (1997). Impairment of calcineurin function in Neurospora crassa reveals its essential role in hyphal growth, morphology and maintenance of the apical Ca2+ gradient. Molecular and General Genetics 256, 104–14.CrossRefGoogle ScholarPubMed
Rayner, A. D. M. (1996). Interconnectedness and individualism in fungal mycelia. In A Century of Mycology, ed. Sutton, B. C., pp. 193–232. Cambridge: Cambridge University Press.Google Scholar
Rayner, A. D. M., Watkins, Z. R. & Beeching, J. R. (1997). Self integration – an emerging concept from the fungal mycelium. In The Fungal Colony, ed. Gow, N. A. R., Robson, G. D. & Gadd, G. M., pp. 1–24. Cambridge: Cambridge University Press.Google Scholar
Read, N. D. (1994). Cellular nature and multicellular morphogenesis of higher fungi. In Shape and Form in Plants and Fungi, ed. Ingram, D. S. & Hudson, A., pp. 251–69. London: Academic Press.Google Scholar
Read, N. D. & Beckett, A. (1996). Ascus and ascospore morphogenesis. Mycological Research 100, 1281–314.CrossRefGoogle Scholar
Read, N. D. & Roca, M. G. (2006). Vegetative hyphal fusion in filamentous fungi. In Cell–Cell Channels, ed. Baluska, F., Volkmann, D. & Barlow, P. W., pp. 87–98. Georgetown, Texas: Landes Bioscience.CrossRefGoogle Scholar
Read, N. D., Kellock, L. J., Knight, H. & Trewavas, A. J. (1992). Contact sensing during infection by fungal pathogens. In Perspectives in Plant Cell Recognition, ed. Callow, J. A. & Green, J. R., pp. 137–172. Cambridge: Cambridge University Press.CrossRefGoogle Scholar
Reynaga-Pena, C. G. & Bartnicki-Garcia, S. (1997). Apical branching in a temperature sensitive mutant of Aspergillus niger. Fungal Genetics and Biology 22, 153–67.CrossRefGoogle Scholar
Riquelme, M., Reynaga-Pena, C. G., Gierz, G. & Bartnicki-Garcia, S. (1998). What determines growth direction in fungal hyphae? Fungal Genetics and Biology 24, 101–9.CrossRefGoogle ScholarPubMed
Robinson, P. M. (1973a). Chemotropism in fungi. Transactions of the British Mycological Society 61, 303–13.CrossRefGoogle Scholar
Robinson, P. M. (1973b). Autotropism in fungal spores and hyphae. Botanical Review 39, 367–84.CrossRefGoogle Scholar
Robinson, P. M. (1973c). Oxygen-positive chemotropic factor for fungi? New Phytologist 72, 1349–56.CrossRefGoogle Scholar
Roca, M. G., Arlt, J., Jeffree, C. E. & Read, N. D. (2005). Cell biology of conidial anastomosis tubes in Neurospora crassa. Eukaryotic Cell 4, 911–19.CrossRefGoogle ScholarPubMed
Schumacher, M. M., Enderlin, C. S. & Selitrennikoff, C. P. (1997). The osmotic-1 locus of Neurospora crassa encodes a putative histidine kinase similar to osmosensors of bacteria and yeast. Current Microbiology 34, 340–7.CrossRefGoogle ScholarPubMed
Snetselaar, K. M., Bolker, M. & Kahmann, R. (1996). Ustilago maydis mating hyphae orient their growth toward pheromone sources. Fungal Genetics and Biology 20, 299–312.CrossRefGoogle ScholarPubMed
Taylor, J. W., Spatafora, J., O'Donnell, K., Lutzoni, F., Hibbet, D. S., Geiser, D., Bruns, T. D. & Blackwell, M. (2004). The Fungi. In Assembling the Tree of Life, ed. Cracraft, J. & Donoghue, M. J., pp. 171–94. Oxford: Oxford University Press.Google Scholar
Tlalka, M., Watkinson, S. C., Darrah, P. R. & Fricker, M. D. (2002). Continuous imaging of amino acid translocation in intact mycelia of Phanerochaete velutina reveals rapid, pulsatile fluxes. New Phytologist 153, 173–84.CrossRefGoogle Scholar
Tlalka, M., Hensman, D., Darrah, P. R., Watkinson, S. C. & Fricker, M. D. (2003). Noncircadian oscillations in amino acid transport have complementary profiles in assimilatory and foraging hyphae of Phanerochaete velutina. New Phytologist 158, 325–35.CrossRefGoogle Scholar
Trinci, A. P. J. (1971). Influence of the width of the peripheral growth zone on the radial growth rate of fungal colonies on solid medium. Journal of General Microbiology 67, 325–44.CrossRefGoogle Scholar
Trinci, A. P. J. (1983). Regulation of hyphal branching and hyphal orientation. In The Ecology and Physiology of the Fungal Mycelium, ed. Jennings, D. H. & Rayner, A. D. M., pp. 243–8. Cambridge, Cambridge University Press.Google Scholar
Tsitsigiannis, D. I., Kowieski, T. M., Zarnowski, R. & Keller, N. P. (2005). Three putative oxylipin biosynthetic genes integrate sexual and asexual development in Aspergillus nidulans. Microbiology 151, 1809–21.CrossRefGoogle ScholarPubMed
Turner, G. & Harris, S. D. (1997). Genetic control of polarized growth and branching in filamentous fungi. In The Fungal Colony, ed. Gow, N. A. R., Robson, G. D. & Gadd, G. M., pp. 229–60. Cambridge: Cambridge University Press.Google Scholar
Ugalde, U. (2006). Autoregulatory signals in mycelial fungi. In The Mycota, vol. 1, Growth, Differentiation and Sexuality, 2nd edn, ed. Kües, U. R. & Fischer, R., pp. 203–213. Berlin: Springer-Verlag.Google Scholar
Yang, Q., Pool, S. I. & Borkovich, K. A. (2002). A G-protein β subunit required for sexual and vegetative development and mainteneance of normal Gα protein levels in Neurospora crassa. Eukaryotic Cell 1, 378–90.CrossRefGoogle Scholar
Zelter, A., Bencina, M., Bowman, B. J., Yarden, O. & Read, N. D. (2004). A comparative genomic analysis of the calcium signaling machinery in Neurospora crassa, Magnaporthe grisea, and Saccharomyces cerevisiae. Fungal Genetics and Biology 41, 827–41.CrossRefGoogle ScholarPubMed
Zhang, Y., Lamm, R., Pillonel, C., Lam, S. & Xu, J. R. (2002). Osmoregulation and fungicide resistance: the Neurospora crassa os-2 gene encodes a HOG1 mitogen-activated protein kinase homologue. Applied and Environmental Microbiology 68, 532–8.CrossRefGoogle ScholarPubMed

Save book to Kindle

To save this book to your Kindle, first ensure coreplatform@cambridge.org is added to your Approved Personal Document E-mail List under your Personal Document Settings on the Manage Your Content and Devices page of your Amazon account. Then enter the ‘name’ part of your Kindle email address below. Find out more about saving to your Kindle.

Note you can select to save to either the @free.kindle.com or @kindle.com variations. ‘@free.kindle.com’ emails are free but can only be saved to your device when it is connected to wi-fi. ‘@kindle.com’ emails can be delivered even when you are not connected to wi-fi, but note that service fees apply.

Find out more about the Kindle Personal Document Service.

Available formats
×

Save book to Dropbox

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Dropbox.

Available formats
×

Save book to Google Drive

To save content items to your account, please confirm that you agree to abide by our usage policies. If this is the first time you use this feature, you will be asked to authorise Cambridge Core to connect with your account. Find out more about saving content to Google Drive.

Available formats
×