Intercalary growth in hyphae of filamentous fungi

Voisey, Christine R.

doi:10.1016/j.fbr.2010.12.001

Cited by 50 publications

(24 citation statements)

References 56 publications

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“…Consistent with this result, the cell wall extension activity measured by extensometry showed a similar distribution pattern for the stipe from the apical region to the basal region. Because stipe specimens were frozen, thawed and compressed to remove the cell sap and eliminate turgor pressure before loading into the extensometer (Cosgrove, 1989), synthetic processes (Bowman & Free, 2006;Kamada et al, 1991;Shioya et al, 2013;Voisey, 2010) and endogenous turgor pressure Money & Ravishankar, 2005) did not contribute to wall extension during measurement. Therefore, wall extension activity reflects wall properties (Cosgrove, 1993).…”

Section: Discussionmentioning

confidence: 99%

“…One of the characteristics of the development of mushroom fruit bodies is stipe elongation growth (Craig et al, 1977;Gruen, 1963;Voisey, 2010), which primarily results from manifold cell elongation (Gooday, 1985;Kamada & Takemaru, 1977;Shioya et al, 2013) rather than cell division as in the intercalary extension of hyphae of endophytic fungi of the genus Epichloë in mutualistic symbiosis with Pooideae grasses (Christensen et al, 2008). Because the stipe cell is surrounded by a wall layer that acts similarly to a straitjacket to constrain and shape the cell, cell elongation requires the irreversible extension of the pre-existing wall to create space for the enlarging protoplast (Bartnicki-Garcia, 1999;Kamada et al, 1991).…”

Section: Introductionmentioning

confidence: 99%

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Characterization of stipe elongation of the mushroom Coprinopsis cinerea

Zhang

Zhou

et al. 2014

Microbiology

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Previously, we observed an acid-induced short-term wall extension in Flammulina velutipes apical stipes during a 15 min period after a change from a neutral to an acidic pH. This acid-induced stipe wall extension was eliminated by heating and reconstituted by a snail expansin-like protein, although we failed to isolate any endogenous expansin-like protein from F. velutipes because of its limited 1 mm fast elongation region. In this study, we report that Coprinopsis cinerea stipes possess a 9 mm fast elongation apical region, which is suitable as a model material for wall extension studies. The elongating apical stipe showed two phases of acid-induced wall extension, an initial quick short-term wall extension during the first 15 min and a slower, gradually decaying long-term wall extension over the subsequent 2 h. After heating or protein inactivation pretreatment, apical stipes lost the long-term wall extension, retaining a slower short-term wall extension, which was reconstituted by an expansin-like snail protein. In contrast, the non-elongating basal stipes showed only a weaker short-term wall extension. We propose that the long-term wall extension is a protein-mediated process involved in stipe elongation, whereas the short-term wall extension is a non-protein mediated process not involved in stipe elongation.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Characterization of stipe elongation of the mushroom Coprinopsis cinerea

Zhang

Zhou

et al. 2014

Microbiology

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“…In contrast to the highly branched hyphal network that forms within tissues of dividing plant cells, hyphae colonizing the intercellular cavities of expanding and differentiating tissue of sheath and blade are restricted in growth, as the number of hyphae do not increase further (Tan et al, 2001;Christensen et al, 2002). Hyphae appear to be tightly attached to the plant cells by an adhesive matrix, so that when plant cells elongate in the leaf expansion zone, hyphae become stretched and switch from tip growth to intercalary growth (Christensen et al, 2008;Voisey, 2010). Intercalary growth of hyphae stops when leaf expansion ceases but the fungus remains metabolically active and hyphal diameter increases (Tan et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

The endophytic symbiont Epichloë festucae establishes an epiphyllous net on the surface of Lolium perenne leaves by development of an expressorium, an appressorium‐like leaf exit structure

Becker

Green

et al. 2016

New Phytologist

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Summary Epichloë festucae forms a mutualistic symbiotic association with Lolium perenne. This biotrophic fungus systemically colonizes the intercellular spaces of aerial tissues to form an endophytic hyphal network. E. festucae also grows as an epiphyte, but the mechanism for leaf surface colonization is not known. Here we identify an appressorium‐like structure, which we call an expressorium that allows endophytic hyphae to penetrate the cuticle from the inside of the leaf to establish an epiphytic hyphal net on the surface of the leaf.We used a combination of scanning electron, transmission electron and confocal laser scanning microscopy to characterize this novel fungal structure and determine the composition of the hyphal cell wall using aniline blue and wheat germ agglutinin labelled with Alexafluor‐488.Expressoria differentiate immediately below the cuticle in the leaf blade and leaf sheath intercalary cell division zones where the hyphae grow by tip growth. Differentiation of this structure requires components of both the NoxA and NoxB NADPH oxidase complexes. Major remodelling of the hyphal cell wall occurs following exit from the leaf.These results establish that the symbiotic association of E. festucae with L. perenne involves an interconnected hyphal network of both endophytic and epiphytic hyphae.

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“…They are notable for their complex biotrophic lifecycle which is synchronized with growth and development of the host from seedling to mature plant. Colonization of the plant by the endophyte proceeds through discrete modes of hyphal growth that alternate between apical extension and branch formation of hyphae in the shoot apical meristem (SAM), intercalary hyphal growth along the length of the filament in expanding host structures, and a phase in mature plant tissues where the fungus stops growing but remains metabolically active (Christensen et al, 2008; Christensen and Voisey, 2009; Voisey, 2010; Eaton et al, 2011). Each phase of vegetative hyphal development is seemingly initiated in response to changes in host development.…”

Section: Introductionmentioning

confidence: 99%

“…For example, the transition between plant cell division and extension in developing leaves correlates with repression of hyphal lateral branch formation and initiation of intercalary hyphal extension; and maturation (cessation of growth) of host leaves correlates with a transition from hyphal intercalary growth to little or no extension or tip (polar) growth. The developmental switch from polar to intercalary hyphal growth is a critical stage in host colonization, and is achieved through initiation of the full cell cycle within intercalary hyphal compartments, including mitosis, the laying down of new septa, and cell expansion, a mechanism of growth rarely observed in vegetative filamentous fungi (Christensen et al, 2008; Christensen and Voisey, 2009; Voisey, 2010). Growth of Epichloë hyphae in plants is therefore restricted to developing plant tissues, particularly those arising from the SAM, axillary meristems (from which new tillers form) and floral meristems; and plant structures undergoing cell expansion such as developing leaves and floral spikes.…”

Section: Introductionmentioning

confidence: 99%

cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

et al. 2016

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The seed-transmitted fungal symbiont, Epichloë festucae, colonizes grasses by infecting host tissues as they form on the shoot apical meristem (SAM) of the seedling. How this fungus accommodates the complexities of plant development to successfully colonize the leaves and inflorescences is unclear. Since adenosine 3′, 5′-cyclic monophosphate (cAMP)-dependent signaling is often essential for host colonization by fungal pathogens, we disrupted the cAMP cascade by insertional mutagenesis of the E. festucae adenylate cyclase gene (acyA). Consistent with deletions of this gene in other fungi, acyA mutants had a slow radial growth rate in culture, and hyphae were convoluted and hyper-branched suggesting that fungal apical dominance had been disrupted. Nitro blue tetrazolium (NBT) staining of hyphae showed that cAMP disruption mutants were impaired in their ability to synthesize superoxide, indicating that cAMP signaling regulates accumulation of reactive oxygen species (ROS). Despite significant defects in hyphal growth and ROS production, E. festucae ΔacyA mutants were infectious and capable of forming symbiotic associations with grasses. Plants infected with E. festucae ΔacyA were marginally less robust than the wild-type (WT), however hyphae were hyper-branched, and leaf tissues heavily colonized, indicating that the tight regulation of hyphal growth normally observed in maturing leaves requires functional cAMP signaling.

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Intercalary growth in hyphae of filamentous fungi

Cited by 50 publications

References 56 publications

Characterization of stipe elongation of the mushroom Coprinopsis cinerea

Characterization of stipe elongation of the mushroom Coprinopsis cinerea

The endophytic symbiont Epichloë festucae establishes an epiphyllous net on the surface of Lolium perenne leaves by development of an expressorium, an appressorium‐like leaf exit structure

cAMP Signaling Regulates Synchronised Growth of Symbiotic Epichloë Fungi with the Host Grass Lolium perenne

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