High air humidity dampens salicylic acid pathway and NPR1 function to promote plant disease

The occurrence of plant disease is determined by interactions among host, pathogen, and environment. Air humidity shapes various aspects of plant physiology and high humidity has long been known to promote numerous phyllosphere diseases. However, the molecular basis of how high humidity interferes w...

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Bibliographic Details
Published in:The EMBO journal 2023-11, Vol.42 (21), p.e113499-n/a
Main Authors: Yao, Lingya, Jiang, Zeyu, Wang, Yiping, Hu, Yezhou, Hao, Guodong, Zhong, Weili, Wan, Shiwei, Xin, Xiu‐Fang
Format: Article
Language:English
Subjects:
Accumulation
Acids
air humidity
Cullin
Defense mechanisms
disease resistance
Down-regulation
Gene expression
Host plants
Host-pathogen interactions
Humidity
NPR1
NPR1 protein
Phyllosphere
Physiological effects
Physiological responses
Physiology
Plant diseases
Plant immunity
Plant physiology
Receptors
sA gene
Salicylic acid
Signal transduction
Ubiquitin-protein ligase
Ubiquitination
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Summary:The occurrence of plant disease is determined by interactions among host, pathogen, and environment. Air humidity shapes various aspects of plant physiology and high humidity has long been known to promote numerous phyllosphere diseases. However, the molecular basis of how high humidity interferes with plant immunity to favor disease has remained elusive. Here we show that high humidity is associated with an “immuno‐compromised” status in Arabidopsis plants. Furthermore, accumulation and signaling of salicylic acid (SA), an important defense hormone, are significantly inhibited under high humidity. NPR1, an SA receptor and central transcriptional co‐activator of SA‐responsive genes, is less ubiquitinated and displays a lower promoter binding affinity under high humidity. The cellular ubiquitination machinery, particularly the Cullin 3‐based E3 ubiquitin ligase mediating NPR1 protein ubiquitination, is downregulated under high humidity. Importantly, under low humidity the Cullin 3a/b mutant plants phenocopy the low SA gene expression and disease susceptibility that is normally observed under high humidity. Our study uncovers a mechanism by which high humidity dampens a major plant defense pathway and provides new insights into the long‐observed air humidity influence on diseases. Synopsis Many plant diseases are more severe when air humidity is high; however, the effect of air humidity on host plant biology remains obscure. This report shows that, in very humid conditions, key salicylic acid‐mediated plant defenses are suppressed, making plants more vulnerable to infection. High humidity triggers a range of plant physiological responses. Investigating the effects of high humidity on individual plant immune pathways revealed a significant suppression of salicylic acid (SA) accumulation and signaling. Cellular ubiquitination pathways are suppressed in high humidity, including the ubiquitination and activity of the SA receptor NPR1. Humidity acts directly on host plants to make them more susceptible to disease.
ISSN:0261-4189
1460-2075
DOI:10.15252/embj.2023113499