Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2012 May 8;109(19):E1192-200.
doi: 10.1073/pnas.1201616109. Epub 2012 Apr 23.

Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

Dong-Lei Yang  1 , Jian Yao, Chuan-Sheng Mei, Xiao-Hong Tong, Long-Jun Zeng, Qun Li, Lang-Tao Xiao, Tai-ping Sun, Jigang Li, Xing-Wang Deng, Chin Mei Lee, Michael F Thomashow, Yinong Yang, Zuhua He, Sheng Yang He
Affiliations

Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade

Dong-Lei Yang et al. Proc Natl Acad Sci U S A. .

Abstract

Plants must effectively defend against biotic and abiotic stresses to survive in nature. However, this defense is costly and is often accompanied by significant growth inhibition. How plants coordinate the fluctuating growth-defense dynamics is not well understood and remains a fundamental question. Jasmonate (JA) and gibberellic acid (GA) are important plant hormones that mediate defense and growth, respectively. Binding of bioactive JA or GA ligands to cognate receptors leads to proteasome-dependent degradation of specific transcriptional repressors (the JAZ or DELLA family of proteins), which, at the resting state, represses cognate transcription factors involved in defense (e.g., MYCs) or growth [e.g. phytochrome interacting factors (PIFs)]. In this study, we found that the coi1 JA receptor mutants of rice (a domesticated monocot crop) and Arabidopsis (a model dicot plant) both exhibit hallmark phenotypes of GA-hypersensitive mutants. JA delays GA-mediated DELLA protein degradation, and the della mutant is less sensitive to JA for growth inhibition. Overexpression of a selected group of JAZ repressors in Arabidopsis plants partially phenocopies GA-associated phenotypes of the coi1 mutant, and JAZ9 inhibits RGA (a DELLA protein) interaction with transcription factor PIF3. Importantly, the pif quadruple (pifq) mutant no longer responds to JA-induced growth inhibition, and overexpression of PIF3 could partially overcome JA-induced growth inhibition. Thus, a molecular cascade involving the COI1-JAZ-DELLA-PIF signaling module, by which angiosperm plants prioritize JA-mediated defense over growth, has been elucidated.

PubMed Disclaimer

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Generation of OsCOI1 RNAi transgenic rice with reduced JA sensitivity. (A) Suppression of OsCOI1a expression in transgenic RNAi lines as shown by RNA blot analysis. A fragment of 825 to 1,244 nt of OsCOI1 was used as the probe, and 25S rRNA was used as the loading control. (B) Suppression of OsCOI1b expression in transgenic RNAi lines as shown by qRT-PCR. (C and D) The representative RNAi lines coi1-13 and coi1-18 show reduced sensitivity to MeJA treatment. Seedlings were grown in one-half MS medium with 0.6% agar supplemented with or without 20 μM MeJA. Pictures were taken at day 7 and shoot length was measured at day 12. Data shown in D are the means from 12 plants. Error bars represent SD. Asterisks indicate significant difference between WT and coi1 mutants based on Student's t test (P < 0.01). (E) Reduced expression of JA-response genes OsMPK7 and OsVSP in coi1-13 and -18 plants revealed by qRT-PCR. Data shown in C and E are the means from two independent experiments. Error bars represent SD. Asterisks indicate the significant difference between WT and coi1 mutants based on Student's t test (P < 0.01).
Fig. 2.
Fig. 2.
Morphological phenotypes of coi1-18 plants. (A) Images of WT (Nipponbare) and coi1-18 plants show plant heights and internode lengths. (B) Quantification of heights of the WT, coi1-13, and coi1-18 plants. More than 30 plants of each line were analyzed. The difference between the control and transgenic plants is significant (**P < 0.001, Student's t test). (C) Lengths of individual internodes in the WT and coi1-18 plants. Each internode of coi1-18 was longer than the counterpart of Nipponbare (*P < 0.01 and **P < 0.001, Student's t test). (D) Microscopic sections of the elongating zone of the uppermost internodes from Nipponbare and coi1-18 grown in the isolated paddy field. (Scale bar, 40 μm.) (E) Cell lengths at the base of the elongating zone of the uppermost internodes in the WT and coi1-18 plants. The cell of coi1-18 is much longer than that of Nipponbare (**P < 0.001, Student's t test).
Fig. 3.
Fig. 3.
The GA-deficiency mutation reverses the phenotype of coi1-18 plants. (A) Morphological phenotype of Eui1-OX/coi1-18. (B) The average plant height of WT, coi1-18, Eui1-OX, and Eui1-OX/coi1-18 plants. (C) The length of each internode of coi1-18 decreased in the Eui1-OX/coi1-18 plants. (D) Expression of OsCOI1 in Eui1-OX/coi1-18. (E and F) Cell lengths at the bases of the uppermost internodes in coi1-18, Eui1-OX/coi1-18, and Eui1-OX plants. (Scale bar, 40 μm.) (G and H) Grain lengths of coi1-18, Eui1-OX/coi1-18, and Eui1-OX plants. Letters on the columns in B, C, F, and H indicate significant differences determined by Tukey–Kramer multiple comparison test (P < 0.05).
Fig. 4.
Fig. 4.
Levels of the rice DELLA protein SLR1 and the antagonistic effect of MeJA on GA-mediated plant growth. (A) The GA-mediated degradation of the DELLA protein SLR1 was promoted in the coi1-18 plants. The 10-d-old seedlings grown on one-half MS plates with 0.6% agar were transferred to liquid one-half MS medium with 100 μM GA3, and the SLR1 protein was detected with an SLR1 antibody at the indicated time points. (B and C) MeJA inhibited GA-induced shoot elongation in WT plants: 1, control plant; and 2 to 5, representative plants treated with GA3 and MeJA in the same order as in Fig. 4C. The relative growth is indicated by the length of second leaf sheath after being treated with 10 μM GA3 and various concentrations of MeJA. (D) MeJA delayed SLR1 degradation induced by GA3. The concentration of GA3 and MeJA used were 10 μM and 100 μM, respectively. (E and F) MeJA inhibited WT rice seedling growth and second sheath elongation in a dose-dependent pattern. Asterisks indicate significant difference between mock and treatments (P < 0.01, Student's t test). (G) MeJA treatment promoted the accumulation of SLR1 in a dose-dependent manner in WT plants. The rice plants were grown on one-half MS plates with 0.6% agar supplemented with MeJA (final concentration indicated on Top).
Fig. 5.
Fig. 5.
The rice slr1 mutant is insensitive to MeJA. (A) WT and slr1 seedling were grown on one-half MS plates with 0.6% agar supplemented with or without 25 μM MeJA. (B) Relative growth of slr1 and WT plants is indicated by percentages of the second leaf sheath lengths with MeJA treatment compared with those without MeJA treatment (**P < 0.001, Student's t test).
Fig. 6.
Fig. 6.
GA-associated phenotypes of the Arabidopsis coi1 mutant and JAZ9 overexpression plants. Image (A) and quantification (B) of petioles of coi1-30 and JAZ9 overexpression plants. The plants were grown in a long-day growth chamber (16 h 120 μmol m−2⋅s−1 light/8 h dark, 22 °C/18 °C). The third true leaves of 21-d-old plants were imaged, and their petiole lengths were measured. Image of 28-d-old plants (C) and quantification (D) of early flowering phenotypes of JAZ9 overexpression lines and coi1-30 plants. The plants were grown under the same conditions as in A. Image (E) and quantification (F) of hypocotyls of coi1-30 and JAZ9 overexpression plants when grown under 10 μmol m−2⋅s−1 continuous white light at 22 °C for 6 d. (Scale bar, 5 mm.) Data shown in B, D, and F are the means from 12 plants. Error bars represent SD. Letters on columns indicate significant differences (P < 0.05, Tukey–Kramer multiple comparison test).
Fig. 7.
Fig. 7.
MeJA increases the level of the Arabidopsis DELLA protein RGA. Seedlings were grown under 10 μmol m−2⋅s−1 continuous white light at 22 °C. (A) Increased accumulation of the RGA protein in Arabidopsis seedlings treated with different concentrations of MeJA for 6 d. RGA and JAZ9 (positive control) were detected by anti-GFP and anti-HA antibody, respectively. (B) MeJA treatment does not affect the RGA transcript level in Arabidopsis. Arabidopsis seedlings were treated with 0.1% ethanol (mock) or 100 μM MeJA for 6 d. Total RNA was purified and used for qRT-PCR analysis. Data shown are the means of three biological replicates. Error bars represent SD. JA-inducible expression of AOS was used as a positive control for JA treatment. Asterisks indicate significant difference between mock and MeJA treatment (P < 0.01, Student's t test).
Fig. 8.
Fig. 8.
JAZ9 interferes with the interaction between RGA and PIF3. (A) 3xHA-JAZ9 interacts with 9xMyc-GAI or 9xMyc-RGA protein when expressed transiently in N. tabacum leaves. Protein extracts were immunoprecipitated with an anti-HA antibody and analyzed by Western blot with an anti-Myc antibody. (B) JAZ9 interacts with RGA protein in 3xHA-JAZ9 transgenic Arabidopsis plants. Protein extracts from 12-d-old seedlings were immunoprecipitated with an anti-HA antibody and analyzed by Western blot with an anti-RGA antibody. (C) JAZ9 inhibits the interaction between RGA and PIF3 in yeast. The activity of the reporter gene HIS3, which indicates the interaction between RGA and PIF3, is greatly reduced [indicated by reduced growth on medium lacking histidine (-His)] in the presence of JAZ9 [induced in medium without methionine (-Met)]. (D) Western blot shows that all proteins analyzed in the Y3H assay (C) were expressed as expected. (E) 3xHA-JAZ9 interferes with the interaction between 9xMyc-RGA and 3xFLAG-PIF3 when transiently expressed in N. tabacum leaves. Protein extracts were immunoprecipitated with an anti-Myc antibody and analyzed by Western blot with anti-FLAG, anti-HA, or anti-Myc antibody.
Fig. 9.
Fig. 9.
JA sensitivity of PIF-overexpressing plants and pif mutants. Seedlings were grown on MS medium with or without 10 μM of MeJA under 10 μmol m−2⋅s−1 continuous white light at 22 °C for 6 d. Image (A) and quantification (B) of the effect of MeJA on Arabidopsis hypocotyl elongation. The hypocotyl lengths were measured and the inhibition of hypocotyl growth was calculated as (1 − treated / untreated) × 100%. Data shown are the means from 16 seedlings. Error bars represent SD. Letters on columns indicate significant differences (P < 0.05, Tukey–Kramer multiple comparison test). (C and D) MeJA has antagonizing effects on the expression of XTH33 (PIF-up-regulated) and EXP10 (down-regulated) genes in Arabidopsis. Total RNAs were purified and used for qRT-PCR analysis. Data shown are the means of three biological replicates. Error bars represent SD. Asterisks indicate significant difference between mock and MeJA treatment (P < 0.05, Student's t test).
Fig. P1.
Fig. P1.
A model illustrating how JA signaling modulates plant growth through antagonizing gibberellin signaling. (A) In coi1 mutant or JAZ-overexpressing plants, JA signaling is down-regulated. Accumulated JAZ repressors titrate DELLA repressors away from PIF transcription factors, allowing more PIFs to activate growth-promoting genes, thereby enhancing growth. (B) Activation of JA signaling in WT plants upon insect or pathogen attacks results in degradation of JAZ repressors and accumulation of DELLA repressors, collectively allowing more DELLA repressors to inhibit PIF transcription factors, thereby slowing growth. Normal JA and gibberellin signaling components are depicted in red and green, respectively, whereas components with reduced level and/or activity are indicated in white. Upward arrows indicate increased level and/or activity, whereas downward arrows indicate reduced level and/or activity. Dashed lines indicate weakened effects.
See this image and copyright information in PMC

Similar articles

See all similar articles

Cited by

See all "Cited by" articles

References

    1. Kazan K, Manners JM. The interplay between light and jasmonate signalling during defence and development. J Exp Bot. 2011;62:4087–4100. - PubMed
    1. Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci. 2012;17:22–31. - PubMed
    1. Browse J. Jasmonate passes muster: A receptor and targets for the defense hormone. Annu Rev Plant Biol. 2009;60:183–205. - PubMed
    1. Fonseca S, et al. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nat Chem Biol. 2009;5:344–350. - PubMed
    1. Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA. COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA. 2008;105:7100–7105. - PMC - PubMed

Publication types

MeSH terms

Associated data