IN BRIEF

Avoiding Shade to Grow Taller but Not Always Stronger: Phytochrome–Jasmonic Acid Interplay

The environment plays a major role in determining whether, when, and how growth occurs, and resource allocation towards growth is an important factor in many contexts. For example, plants whose defenses against pathogens are activated often grow less, and plants that must grow taller to reach the light in crowded and shaded conditions can be compromised in defense. The balance between growth and defense in plants has been known for decades (for a review, see Huot et al. 2014), but the precise interplay of these factors in shade conditions, specifically, and the incorporation of light and hormones into these phenomena⎯leading to potentially complex crosstalk among these pathways⎯have yet to be examined in depth. Liu et al. (2019) have made headway in this area, elegantly demonstrating, in a series of experiments testing various genetic and physical interactions among molecular players in Arabidopsis thaliana, the connection between phytochrome and jasmonic acid (JA) signaling pathways in the shade avoidance syndrome, via the interaction of FAR-RED ELONGATED HYPOCOTYLS3 (FHY3) and FAR-RED-IMPAIRED RESPONSE1 (FAR1) transcription factors with JAZ proteins.

In light with a low red–to–far-red ratio (R/FR), i.e., shade, which signals to plants that other plants are nearby and preferentially absorbing red light for photosynthesis, wild-type (WT) plants grow tall, but there is such a thing as being too tall. In the shade, the fhy3 single and fhy3 far1 double loss-of-function mutants grew even taller (via increased cell length) than WT, and lost the ability to repress growth in response to JA (see figure), just like a JAZ1 overexpressor line and the coi1 mutant that is defective in JA perception. Shade-induced marker genes were also significantly more upregulated in these plants with excessively elongated hypocotyls, and fhy3 far1 mutants specifically exhibited an overall downregulation of stress-response genes and a marked reduction in the upregulation of JA genes as compared to WT plants, in shade, independent of JA treatment (see figure). While WT plants were more susceptible to the necrotrophic fungus Botrytis cinerea in the shade as compared to in high R/FR light, fhy3 and fhy3 far1 mutants were

even more susceptible, in both shade and non-shade conditions (see figure).

On a mechanistic level, Liu et al. (2019) provide molecular evidence suggesting that normally, in shade conditions, FHY3 and FAR1, which activate phytochrome responses to far-red light, bind to the promoters and increase the expression of the PAR1 and PAR2 genes to reduce excessive growth, and also bind to MYC2, MYC3, and MYC4 to help induce the expression of JA-mediated defense genes. JAZ proteins, inhibitors of JA signaling, directly bind to and counteract FHY3 and FAR1 activity, causing reduced JA-mediated defenses and simultaneous increased growth.

These results support a proposed role for FHY3 and FAR1 in JA-mediated defense, and importantly, support the notion that being too tall can make plants even more susceptible to some stresses. While JA promotes defense against necrotrophic pathogens and insect herbivory, salicylic acid (SA), which counteracts JA, promotes defense against biotrophs. Therefore, it is interesting to speculate as to whether, during shade avoidance, resistance against necrotrophs is independent of SA, and how the various hormone pathways are coordinated to effect resistance to other pathogens. Only time (and shade!) will tell.

Anne C. Rea Michigan State University

MSU-DOE Plant Research Laboratory acr32@cornell.edu

ORCID: 0000-0002-2996-5709

REFERENCES Huot B., Yao J., Montgomery B.L., and He S.Y. (2014). Growth–defense tradeoffs in

plants: A balancing act to optimize fitness. Mol. Plant 7: 1267–1287.

Liu Y., Wei H., Ma M., Li Q., Kong D., Sun J., Ma X., Wang B., Chen C., Xie Y., and Wang H. (2019). Arabidopsis FHY3 and FAR1 proteins regulate the balance between growth and defense under shade conditions. Plant Cell. DOI: https://doi.org/10.1105/tpc.18.00991.

Phytochrome signaling genes are involved in keeping plants from being simultaneously too tall and too susceptible to necrotrophs in the shade. fhy3 and fhy3 far1 mutants display excessively long hypocotyl (cell) lengths in low (L) red–to–far-red light, are insensitive to jasmonic acid (JA) treatment, and exhibit increased susceptibility to necrotrophic pathogens. [Adapted from Liu et al. (2019), Figures 3 and 7.]

Figure 3. The fhy3 and fhy3 far1 Mutants Are Less Sensitive to JA-mediated Repression ofHypocotyl Elongation(A) and (B) Visual image(A) and quantification (B) of the effect of JA on hypocotyl elongation of wild typeseedlings grown under simulated shade. 3-day-old seedlings were either kept in high R/FR or transferredto simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM) for 3 days. Different lettersindicate significant differences by one-way ANOVA analysis with SAS software (P < 0.05). Data arepresented as the means ± SD, n>15.(C) and (D) Phenotypic analysis of the effect of JA on hypocotyl cell elongation of of wild type seedlingsgrown under simulated shade. Representative images of hypocotyl cell are shown in (C). White scale barrepresents 200 μm. Quantification of cell length is shown in (D). Data are means ± SD, including >50 cellsfrom three to four independent seedlings.(E) Quantitative RT-PCR analysis of IAA29, HFR1, YUC8 and PRE1 expression in wild-type seedlingsgrown in white light or simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM). Dataare presented as the means ± SD, n=3.(F) and (G) Representative images (F) and quantification (G) of the effect of JA on wild-type, fhy3-11 and fhy3-11 far1-4 seedlings grown under simulated shade with or without 20 μM JA. White scale barrepresents 2 mm. (**P < 0.01, Student’s t test, n.s. no significance). Data are presented as the means ±SD, n>15.

Figure 3. The fhy3 and fhy3 far1 Mutants Are Less Sensitive to JA-mediated Repression ofHypocotyl Elongation(A) and (B) Visual image(A) and quantification (B) of the effect of JA on hypocotyl elongation of wild typeseedlings grown under simulated shade. 3-day-old seedlings were either kept in high R/FR or transferredto simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM) for 3 days. Different lettersindicate significant differences by one-way ANOVA analysis with SAS software (P < 0.05). Data arepresented as the means ± SD, n>15.(C) and (D) Phenotypic analysis of the effect of JA on hypocotyl cell elongation of of wild type seedlingsgrown under simulated shade. Representative images of hypocotyl cell are shown in (C). White scale barrepresents 200 μm. Quantification of cell length is shown in (D). Data are means ± SD, including >50 cellsfrom three to four independent seedlings.(E) Quantitative RT-PCR analysis of IAA29, HFR1, YUC8 and PRE1 expression in wild-type seedlingsgrown in white light or simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM). Dataare presented as the means ± SD, n=3.(F) and (G) Representative images (F) and quantification (G) of the effect of JA on wild-type, fhy3-11 and fhy3-11 far1-4 seedlings grown under simulated shade with or without 20 μM JA. White scale barrepresents 2 mm. (**P < 0.01, Student’s t test, n.s. no significance). Data are presented as the means ±SD, n>15.

A

C

Figure 3. The fhy3 and fhy3 far1 Mutants Are Less Sensitive to JA-mediated Repression ofHypocotyl Elongation(A) and (B) Visual image(A) and quantification (B) of the effect of JA on hypocotyl elongation of wild typeseedlings grown under simulated shade. 3-day-old seedlings were either kept in high R/FR or transferredto simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM) for 3 days. Different lettersindicate significant differences by one-way ANOVA analysis with SAS software (P < 0.05). Data arepresented as the means ± SD, n>15.(C) and (D) Phenotypic analysis of the effect of JA on hypocotyl cell elongation of of wild type seedlingsgrown under simulated shade. Representative images of hypocotyl cell are shown in (C). White scale barrepresents 200 μm. Quantification of cell length is shown in (D). Data are means ± SD, including >50 cellsfrom three to four independent seedlings.(E) Quantitative RT-PCR analysis of IAA29, HFR1, YUC8 and PRE1 expression in wild-type seedlingsgrown in white light or simulated shade with different concentration of JA (0, 10 μM, 50 μM, 100 μM). Dataare presented as the means ± SD, n=3.(F) and (G) Representative images (F) and quantification (G) of the effect of JA on wild-type, fhy3-11 and fhy3-11 far1-4 seedlings grown under simulated shade with or without 20 μM JA. White scale barrepresents 2 mm. (**P < 0.01, Student’s t test, n.s. no significance). Data are presented as the means ±SD, n>15.

B

Figure 7. The fhy3 far1 Mutant Are More Susceptible to B. cinerea Under Simulated Shade(A) Histichemical staining of the 35S::GUS-FHY3 seedlings (10-day-old) treated with 100 μM JA or equalvolume of ethanol (Mock) for 10 h.(B) Immunoblot assay shows that JA promotes accumulation of FHY3 protein. 5-day-old 35S::FLAG-FHY3-HA seedlings were treated with 50 μM JA for the indicated time. FHY3 protein was detected withanti-FLAG antibody (1: 4,000; MBL). Tubulin was used as a loading control.(C) Immunoblot assay shows that accumulation of FHY3 protein decreased in the 35S::FHY3-FLAGJAZ1OE seedlings treated with low R/FR for the indicated time.(D) Disease symptoms of wild type and fhy3-11 far1-4 plants incubated with B. cinerea. 4-week-oldrosette leaves were incubated with 5 × 105 spores/mL and then placed under white light or simulatedshade for 2 d before observation.(E) Quantification of the lesion areas on rosette leaves after inoculation with B. cinerea spores. Differentletters denote statistically significant differences by one-way ANOVA analysis (p < 0.05). Data are themeans ± SD, three independent experiments with similar results.(F-I) Quantitative RT-PCR analysis of JA responsive genes (LOX2, PDF1.2, TAT1, and VSP2) in wild-type,coi1-2 and fhy3-11 far1-4 plants grown under simulated shade conditions with or without JA application for3 days. Asterisks indicate significant differences between indicated means with P<0.05 by Student’s t test.Data are means ± SD, n=3.

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Plant Cell Advance Publication. Published on August 7, 2019, doi:10.1105/tpc.19.00599

©2019 American Society of Plant Biologists. All Rights Reserved

DOI 10.1105/tpc.19.00599; originally published online August 7, 2019;Plant Cell

Anne C. ReaAvoiding Shade to Grow Taller but Not Always Stronger: Phytochrome-Jasmonic Acid Interplay

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