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Arbuscular mycorrhizal fungi trigger danger-associated peptide signaling and inhibit carbon‒phosphorus exchange with nonhost plants

Wang, Yutao ; Chen, Hanwen ; Shao, Meishuang ; Zhu, Ting ; Li, Shaoshan ; Olsson, Pål Axel LU and Hammer, Edith C. LU (2023) In Plant Cell and Environment 46(7). p.2206-2221
Abstract

In soil, arbuscular mycorrhizal fungi (AMF) meet the roots of both host and presumed nonhost plants, but the interactional mechanisms of AMF with and functional relevance for nonhost plants is little known. Here we show AMF can colonize an individually grown nonhost plant, Arabidopsis thaliana, and suppress the growth of Arabidopsis and two nonhost Brassica crops. This inhibitory effect increased with increasing AMF inoculum density, and was independent of AMF species or nutrient availability. 13C isotope labeling and physiological analyses revealed no significant carbon‒phosphorus exchange between Arabidopsis and AMF, indicating a lack of nutritional function in this interaction. AMF colonization activated the... (More)

In soil, arbuscular mycorrhizal fungi (AMF) meet the roots of both host and presumed nonhost plants, but the interactional mechanisms of AMF with and functional relevance for nonhost plants is little known. Here we show AMF can colonize an individually grown nonhost plant, Arabidopsis thaliana, and suppress the growth of Arabidopsis and two nonhost Brassica crops. This inhibitory effect increased with increasing AMF inoculum density, and was independent of AMF species or nutrient availability. 13C isotope labeling and physiological analyses revealed no significant carbon‒phosphorus exchange between Arabidopsis and AMF, indicating a lack of nutritional function in this interaction. AMF colonization activated the danger-associated peptide Pep-PEPR signaling pathway, and caused clear defense responses in Arabidopsis. The impairment of Pep-PEPR signaling in nonhost plants greatly compromised AMF-triggered defensive responses and photosynthesis suppression, leading to higher colonization rates and reduced growth suppression upon AMF inoculation. Pretreatment with Pep peptide decreased AMF colonization, and largely substituted for AMF-induced growth suppression in nonhosts, confirming that the Pep-PEPR pathway is a key participant in resistance to AMF colonization and in mediating growth suppression of nonhost plants. This work greatly increases our knowledge about the functional relevance of AMF and their mechanisms of interactions with nonhost plants.

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author
; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Arabidopsis thaliana, arbuscular mycorrhizal fungi (AMF), carbon and phosphorus exchange, danger/damage-associated molecular patterns (DAMP), nonhost (nonmycorrhizal) plants, plant elicitor peptide (Pep)
in
Plant Cell and Environment
volume
46
issue
7
pages
16 pages
publisher
Wiley-Blackwell
external identifiers
  • pmid:37151160
  • scopus:85158129862
ISSN
0140-7791
DOI
10.1111/pce.14600
language
English
LU publication?
yes
id
b1e69322-70f4-4feb-ae96-fe5af3b20f0d
date added to LUP
2023-08-16 08:50:06
date last changed
2024-04-20 00:43:01
@article{b1e69322-70f4-4feb-ae96-fe5af3b20f0d,
  abstract     = {{<p>In soil, arbuscular mycorrhizal fungi (AMF) meet the roots of both host and presumed nonhost plants, but the interactional mechanisms of AMF with and functional relevance for nonhost plants is little known. Here we show AMF can colonize an individually grown nonhost plant, Arabidopsis thaliana, and suppress the growth of Arabidopsis and two nonhost Brassica crops. This inhibitory effect increased with increasing AMF inoculum density, and was independent of AMF species or nutrient availability. <sup>13</sup>C isotope labeling and physiological analyses revealed no significant carbon‒phosphorus exchange between Arabidopsis and AMF, indicating a lack of nutritional function in this interaction. AMF colonization activated the danger-associated peptide Pep-PEPR signaling pathway, and caused clear defense responses in Arabidopsis. The impairment of Pep-PEPR signaling in nonhost plants greatly compromised AMF-triggered defensive responses and photosynthesis suppression, leading to higher colonization rates and reduced growth suppression upon AMF inoculation. Pretreatment with Pep peptide decreased AMF colonization, and largely substituted for AMF-induced growth suppression in nonhosts, confirming that the Pep-PEPR pathway is a key participant in resistance to AMF colonization and in mediating growth suppression of nonhost plants. This work greatly increases our knowledge about the functional relevance of AMF and their mechanisms of interactions with nonhost plants.</p>}},
  author       = {{Wang, Yutao and Chen, Hanwen and Shao, Meishuang and Zhu, Ting and Li, Shaoshan and Olsson, Pål Axel and Hammer, Edith C.}},
  issn         = {{0140-7791}},
  keywords     = {{Arabidopsis thaliana; arbuscular mycorrhizal fungi (AMF); carbon and phosphorus exchange; danger/damage-associated molecular patterns (DAMP); nonhost (nonmycorrhizal) plants; plant elicitor peptide (Pep)}},
  language     = {{eng}},
  number       = {{7}},
  pages        = {{2206--2221}},
  publisher    = {{Wiley-Blackwell}},
  series       = {{Plant Cell and Environment}},
  title        = {{Arbuscular mycorrhizal fungi trigger danger-associated peptide signaling and inhibit carbon‒phosphorus exchange with nonhost plants}},
  url          = {{http://dx.doi.org/10.1111/pce.14600}},
  doi          = {{10.1111/pce.14600}},
  volume       = {{46}},
  year         = {{2023}},
}