Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis

Hye Seon Kim, Kirk J. Czymmek, Agam Patel, Shannon Modla, Anja Nohe, Randall Duncan, Simon Gilroy, Seogchan Kang

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

Calcium is a universal messenger that translates diverse environmental stimuli and developmental cues into specific cellular and developmental responses. While individual fungal species have evolved complex and often unique biochemical and structural mechanisms to exploit specific ecological niches and to adjust growth and development in response to external stimuli, one universal feature to all is that Ca2+-mediated signaling is involved. The lack of a robust method for imaging spatial and temporal dynamics of subcellular Ca2+ (i.e., " Ca2+ signature" ), readily available in the plant and animal systems, has severely limited studies on how this signaling pathway controls fungal growth, development, and pathogenesis. Here, we report the first successful expression of a FRET (Förster Resonance Energy Transfer)-based Ca2+ biosensor in fungi. Time-lapse imaging of Magnaporthe oryzae, Fusarium oxysporum, and Fusarium graminearum expressing this sensor showed that instead of a continuous gradient, the cytoplasmic Ca2+ ([Ca2+]c) change occurred in a pulsatile manner with no discernable gradient between pulses, and each species exhibited a distinct Ca2+ signature. Furthermore, occurrence of pulsatile Ca2+ signatures was age and development dependent, and major [Ca2+]c transients were observed during hyphal branching, septum formation, differentiation into specialized plant infection structures, cell-cell contact and in planta growth. In combination with the sequenced genomes and ease of targeted gene manipulation of these and many other fungal species, the data, materials and methods developed here will help understand the mechanism underpinning Ca2+-mediated control of cellular and developmental changes, its role in polarized growth forms and the evolution of Ca2+ signaling across eukaryotic kingdoms.

Original languageEnglish (US)
Pages (from-to)589-601
Number of pages13
JournalFungal Genetics and Biology
Volume49
Issue number8
DOIs
StatePublished - Aug 1 2012

Fingerprint

Fusarium
Biosensing Techniques
Growth and Development
Fungi
Magnaporthe
Time-Lapse Imaging
Calcium
Plant Structures
Energy Transfer
Growth
Cues
Genome
Infection
Genes
Oryza

All Science Journal Classification (ASJC) codes

  • Microbiology
  • Genetics

Cite this

Kim, Hye Seon ; Czymmek, Kirk J. ; Patel, Agam ; Modla, Shannon ; Nohe, Anja ; Duncan, Randall ; Gilroy, Simon ; Kang, Seogchan. / Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis. In: Fungal Genetics and Biology. 2012 ; Vol. 49, No. 8. pp. 589-601.
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Expression of the Cameleon calcium biosensor in fungi reveals distinct Ca2+ signatures associated with polarized growth, development, and pathogenesis. / Kim, Hye Seon; Czymmek, Kirk J.; Patel, Agam; Modla, Shannon; Nohe, Anja; Duncan, Randall; Gilroy, Simon; Kang, Seogchan.

In: Fungal Genetics and Biology, Vol. 49, No. 8, 01.08.2012, p. 589-601.

Research output: Contribution to journalArticle

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