IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses

Adrian A. Moreno, M. Shahid Mukhtar, Francisca Blanco, Jon Lucas Boatwright, Ignacio Moreno, Melissa R. Jordan, Yani Chen, Federica Brandizzi, Xinnian Dong, Ariel Orellana, Karolina M. Pajerowska-Mukhtar

Resultado de la investigación: Article

101 Citas (Scopus)

Resumen

Endoplasmic reticulum (ER)-mediated protein secretion and quality control have been shown to play an important role in immune responses in both animals and plants. In mammals, the ER membrane-located IRE1 kinase/endoribonuclease, a key regulator of unfolded protein response (UPR), is required for plasma cell development to accommodate massive secretion of immunoglobulins. Plant cells can secrete the so-called pathogenesis-related (PR) proteins with antimicrobial activities upon pathogen challenge. However, whether IRE1 plays any role in plant immunity is not known. Arabidopsis thaliana has two copies of IRE1, IRE1a and IRE1b. Here, we show that both IRE1a and IRE1b are transcriptionally induced during chemically-induced ER stress, bacterial pathogen infection and treatment with the immune signal salicylic acid (SA). However, we found that IRE1a plays a predominant role in the secretion of PR proteins upon SA treatment. Consequently, the ire1a mutant plants show enhanced susceptibility to a bacterial pathogen and are deficient in establishing systemic acquired resistance (SAR), whereas ire1b is unaffected in these responses. We further demonstrate that the immune deficiency in ire1a is due to a defect in SA- and pathogen-triggered, IRE1-mediated cytoplasmic splicing of the bZIP60 mRNA, which encodes a transcription factor involved in the expression of UPR-responsive genes. Consistently, IRE1a is preferentially required for bZIP60 splicing upon pathogen infection, while IRE1b plays a major role in bZIP60 processing upon Tunicamycin (Tm)-induced stress. We also show that SA-dependent induction of UPR-responsive genes is altered in the bzip60 mutant resulting in a moderate susceptibility to a bacterial pathogen. These results indicate that the IRE1/bZIP60 branch of UPR is a part of the plant response to pathogens for which the two Arabidopsis IRE1 isoforms play only partially overlapping roles and that IRE1 has both bZIP60-dependent and bZIP60-independent functions in plant immunity.

Idioma originalEnglish
Número de artículoe31944
PublicaciónPLoS ONE
Volumen7
N.º2
DOI
EstadoPublished - 16 feb 2012

Huella dactilar

Plant Immunity
unfolded protein response
Unfolded Protein Response
Salicylic Acid
Pathogens
abiotic stress
stress response
immunity
pathogens
salicylic acid
Arabidopsis
Endoplasmic Reticulum
Proteins
endoplasmic reticulum
Endoribonucleases
pathogenesis-related proteins
Tunicamycin
Endoplasmic Reticulum Stress
Plant Cells
Plasma Cells

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Citar esto

Moreno, Adrian A. ; Mukhtar, M. Shahid ; Blanco, Francisca ; Boatwright, Jon Lucas ; Moreno, Ignacio ; Jordan, Melissa R. ; Chen, Yani ; Brandizzi, Federica ; Dong, Xinnian ; Orellana, Ariel ; Pajerowska-Mukhtar, Karolina M. / IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. En: PLoS ONE. 2012 ; Vol. 7, N.º 2.
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title = "IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses",
abstract = "Endoplasmic reticulum (ER)-mediated protein secretion and quality control have been shown to play an important role in immune responses in both animals and plants. In mammals, the ER membrane-located IRE1 kinase/endoribonuclease, a key regulator of unfolded protein response (UPR), is required for plasma cell development to accommodate massive secretion of immunoglobulins. Plant cells can secrete the so-called pathogenesis-related (PR) proteins with antimicrobial activities upon pathogen challenge. However, whether IRE1 plays any role in plant immunity is not known. Arabidopsis thaliana has two copies of IRE1, IRE1a and IRE1b. Here, we show that both IRE1a and IRE1b are transcriptionally induced during chemically-induced ER stress, bacterial pathogen infection and treatment with the immune signal salicylic acid (SA). However, we found that IRE1a plays a predominant role in the secretion of PR proteins upon SA treatment. Consequently, the ire1a mutant plants show enhanced susceptibility to a bacterial pathogen and are deficient in establishing systemic acquired resistance (SAR), whereas ire1b is unaffected in these responses. We further demonstrate that the immune deficiency in ire1a is due to a defect in SA- and pathogen-triggered, IRE1-mediated cytoplasmic splicing of the bZIP60 mRNA, which encodes a transcription factor involved in the expression of UPR-responsive genes. Consistently, IRE1a is preferentially required for bZIP60 splicing upon pathogen infection, while IRE1b plays a major role in bZIP60 processing upon Tunicamycin (Tm)-induced stress. We also show that SA-dependent induction of UPR-responsive genes is altered in the bzip60 mutant resulting in a moderate susceptibility to a bacterial pathogen. These results indicate that the IRE1/bZIP60 branch of UPR is a part of the plant response to pathogens for which the two Arabidopsis IRE1 isoforms play only partially overlapping roles and that IRE1 has both bZIP60-dependent and bZIP60-independent functions in plant immunity.",
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Moreno, AA, Mukhtar, MS, Blanco, F, Boatwright, JL, Moreno, I, Jordan, MR, Chen, Y, Brandizzi, F, Dong, X, Orellana, A & Pajerowska-Mukhtar, KM 2012, 'IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses', PLoS ONE, vol. 7, n.º 2, e31944. https://doi.org/10.1371/journal.pone.0031944

IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. / Moreno, Adrian A.; Mukhtar, M. Shahid; Blanco, Francisca; Boatwright, Jon Lucas; Moreno, Ignacio; Jordan, Melissa R.; Chen, Yani; Brandizzi, Federica; Dong, Xinnian; Orellana, Ariel; Pajerowska-Mukhtar, Karolina M.

En: PLoS ONE, Vol. 7, N.º 2, e31944, 16.02.2012.

Resultado de la investigación: Article

TY - JOUR

T1 - IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses

AU - Moreno, Adrian A.

AU - Mukhtar, M. Shahid

AU - Blanco, Francisca

AU - Boatwright, Jon Lucas

AU - Moreno, Ignacio

AU - Jordan, Melissa R.

AU - Chen, Yani

AU - Brandizzi, Federica

AU - Dong, Xinnian

AU - Orellana, Ariel

AU - Pajerowska-Mukhtar, Karolina M.

PY - 2012/2/16

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