Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco

Petri Lackman, Miguel González-Guzmán, Sofie Tilleman, Inês Carqueijeiro, Amparo Cuéllar Pérez, Tessa Moses, Mitsunori Seo, Yuri Kanno, Suvi T. Häkkinen, Marc C. E. Van Montagu (Corresponding Author), Johan M. Thevelein, Hannu Maaheimo, Kirsi-Marja Oksman-Caldentey, Pedro L. Rodriguez, Heiko Rischer, Alain Goossens (Corresponding Author)

Research output: Contribution to journalArticleScientificpeer-review

122 Citations (Scopus)

Abstract

The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.
Original languageEnglish
Pages (from-to)5891-5896
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number14
DOIs
Publication statusPublished - 2011
MoE publication typeA1 Journal article-refereed

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abscisic acid
tobacco
Arabidopsis
receptors
alkaloids
biochemical pathways
jasmonic acid
plant hormones
Nicotiana tabacum
anthocyanins
Arabidopsis thaliana
biosynthesis
metabolism
biomass
genes
proteins

Keywords

  • nicotine
  • phenylpropanoid
  • primary metabolism
  • secondary metabolism
  • stress response

Cite this

Lackman, Petri ; González-Guzmán, Miguel ; Tilleman, Sofie ; Carqueijeiro, Inês ; Cuéllar Pérez, Amparo ; Moses, Tessa ; Seo, Mitsunori ; Kanno, Yuri ; Häkkinen, Suvi T. ; Van Montagu, Marc C. E. ; Thevelein, Johan M. ; Maaheimo, Hannu ; Oksman-Caldentey, Kirsi-Marja ; Rodriguez, Pedro L. ; Rischer, Heiko ; Goossens, Alain. / Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. In: Proceedings of the National Academy of Sciences of the United States of America. 2011 ; Vol. 108, No. 14. pp. 5891-5896.
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title = "Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco",
abstract = "The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.",
keywords = "nicotine, phenylpropanoid, primary metabolism, secondary metabolism, stress response",
author = "Petri Lackman and Miguel Gonz{\'a}lez-Guzm{\'a}n and Sofie Tilleman and In{\^e}s Carqueijeiro and {Cu{\'e}llar P{\'e}rez}, Amparo and Tessa Moses and Mitsunori Seo and Yuri Kanno and H{\"a}kkinen, {Suvi T.} and {Van Montagu}, {Marc C. E.} and Thevelein, {Johan M.} and Hannu Maaheimo and Kirsi-Marja Oksman-Caldentey and Rodriguez, {Pedro L.} and Heiko Rischer and Alain Goossens",
year = "2011",
doi = "10.1073/pnas.1103010108",
language = "English",
volume = "108",
pages = "5891--5896",
journal = "Proceedings of the National Academy of Sciences of the United States of America",
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Lackman, P, González-Guzmán, M, Tilleman, S, Carqueijeiro, I, Cuéllar Pérez, A, Moses, T, Seo, M, Kanno, Y, Häkkinen, ST, Van Montagu, MCE, Thevelein, JM, Maaheimo, H, Oksman-Caldentey, K-M, Rodriguez, PL, Rischer, H & Goossens, A 2011, 'Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 14, pp. 5891-5896. https://doi.org/10.1073/pnas.1103010108

Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. / Lackman, Petri; González-Guzmán, Miguel; Tilleman, Sofie; Carqueijeiro, Inês; Cuéllar Pérez, Amparo; Moses, Tessa; Seo, Mitsunori; Kanno, Yuri; Häkkinen, Suvi T.; Van Montagu, Marc C. E. (Corresponding Author); Thevelein, Johan M.; Maaheimo, Hannu; Oksman-Caldentey, Kirsi-Marja; Rodriguez, Pedro L.; Rischer, Heiko; Goossens, Alain (Corresponding Author).

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 14, 2011, p. 5891-5896.

Research output: Contribution to journalArticleScientificpeer-review

TY - JOUR

T1 - Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco

AU - Lackman, Petri

AU - González-Guzmán, Miguel

AU - Tilleman, Sofie

AU - Carqueijeiro, Inês

AU - Cuéllar Pérez, Amparo

AU - Moses, Tessa

AU - Seo, Mitsunori

AU - Kanno, Yuri

AU - Häkkinen, Suvi T.

AU - Van Montagu, Marc C. E.

AU - Thevelein, Johan M.

AU - Maaheimo, Hannu

AU - Oksman-Caldentey, Kirsi-Marja

AU - Rodriguez, Pedro L.

AU - Rischer, Heiko

AU - Goossens, Alain

PY - 2011

Y1 - 2011

N2 - The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.

AB - The phytohormones jasmonates (JAs) constitute an important class of elicitors for many plant secondary metabolic pathways. However, JAs do not act independently but operate in complex networks with crosstalk to several other phytohormonal signaling pathways. Here, crosstalk was detected between the JA and abscisic acid (ABA) signaling pathways in the regulation of tobacco (Nicotiana tabacum) alkaloid biosynthesis. A tobacco gene from the PYR/PYL/RCAR family, NtPYL4, the expression of which is regulated by JAs, was found to encode a functional ABA receptor. NtPYL4 inhibited the type-2C protein phosphatases known to be key negative regulators of ABA signaling in an ABA-dependent manner. Overexpression of NtPYL4 in tobacco hairy roots caused a reprogramming of the cellular metabolism that resulted in a decreased alkaloid accumulation and conferred ABA sensitivity to the production of alkaloids. In contrast, the alkaloid biosynthetic pathway was not responsive to ABA in control tobacco roots. Functional analysis of the Arabidopsis (Arabidopsis thaliana) homologs of NtPYL4, PYL4 and PYL5, indicated that also in Arabidopsis altered PYL expression affected the JA response, both in terms of biomass and anthocyanin production. These findings define a connection between a component of the core ABA signaling pathway and the JA responses and contribute to the understanding of the role of JAs in balancing tradeoffs between growth and defense.

KW - nicotine

KW - phenylpropanoid

KW - primary metabolism

KW - secondary metabolism

KW - stress response

U2 - 10.1073/pnas.1103010108

DO - 10.1073/pnas.1103010108

M3 - Article

VL - 108

SP - 5891

EP - 5896

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

SN - 0027-8424

IS - 14

ER -