Research ArticlePlant biology

Coordinating the overall stomatal response of plants: Rapid leaf-to-leaf communication during light stress

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Science Signaling  20 Feb 2018:
Vol. 11, Issue 518, eaam9514
DOI: 10.1126/scisignal.aam9514
  • Fig. 1 Local application of light stress triggers a local and systemic stomatal closure response in Arabidopsis.

    (A) The experimental design used to measure stomatal responses and changes in steady-state transcript levels in response to local application of light stress. Each sampled leaf was divided along its mid vain and used for stomatal aperture measurements and determination of Zat12 expression. (B) Local and systemic stomatal aperture response of Arabidopsis to local application of light stress (high light; HL). n = 500 stomata from 30 different plants for each group. (C) Changes in the steady-state levels of the rapid systemic response transcript Zat12 in local and systemic leaves after application of light stress to a local leaf. n = 30 plants for each group. (D) Local and systemic stomatal aperture response of Arabidopsis mutants lacking the respiratory burst oxidase homolog D enzyme (rbohD) to local application of light stress (high light; HL). n = 500 stomata from 30 different plants for each group. (E) The experimental design used to measure canopy-wide systemic stomatal responses to local application of light stress (left) and bar graphs showing the systemic stomatal aperture response of six different systemic leaves (S1 to S6) in response to light stress application to a local leaf (local, right). n = 500 stomata from 30 different plants for each group. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE, ***P < 0.005, **P < 0.01, and *P < 0.05.

  • Fig. 2 Inhibition of reactive oxygen or calcium signaling blocks the signal that mediates the rapid systemic stomatal closure response in Arabidopsis.

    (A) The experimental procedure used to block the systemic signal using different inhibitors and to measure stomatal responses and reactive oxygen species (ROS) accumulation. (B) Effect of diphenyleneiodonium (DPI; 50 μM) application on the systemic stomatal aperture response to local application of light stress. n = 500 stomata from 30 different plants for each group. (C) Effect of DPI (50 μM) application on the systemic H2O2 accumulation response of Arabidopsis to local application of light stress. n = 30 plants for each group. (D) Effect of LaCl3 application on the systemic stomatal aperture response of Arabidopsis to local application of light stress. n = 500 stomata from 30 different plants for each group. (E) Response of Zat12::Luciferase reporter plants to local application of light stress. n = 30 plants for each group. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE. ***P < 0.005, **P < 0.01, *P < 0.05.

  • Fig. 3 Application of ABA to a local leaf triggers local and systemic stomatal closure responses.

    (A) The experimental procedure used to measure local and systemic stomatal aperture responses to local application of abscisic acid (ABA) (50 μM) in Arabidopsis. (B) Local and systemic stomatal aperture response to local application of ABA. n = 500 stomata from 30 different plants for each group. (C) Bar graphs showing the effect of DPI (50 μM) application (as in Fig. 2A) on the systemic stomatal aperture response of Arabidopsis to local application of ABA. n = 500 stomata from 30 different plants for each group. (D) The response of Zat12::Luciferase reporter plants to local application of ABA (50 μM). n = 30 plants for each group. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE, ***P < 0.005, **P < 0.01, and *P < 0.05.

  • Fig. 4 ABA is required to trigger the local and systemic stomatal closure response of Arabidopsis to local application of light stress.

    (A) ABA concentrations in local and systemic leaves of untreated Arabidopsis plants grown under control conditions (C) or subjected to high relative humidity (80 to 85%; HH). n = 30 plants for each group. (B) Local and systemic stomatal closure response of Arabidopsis plants subjected to light stress (applied to a local leaf) under conditions of high humidity. n = 500 stomata from 30 different plants for each group. (C) Local and systemic H2O2 accumulation response of Arabidopsis plants subjected to light stress (applied to a local leaf) under conditions of high humidity. n = 30 plants for each group. (D) Local and systemic stomatal closure response of wild-type Arabidopsis (Col or Ler) to local application of light stress. n = 500 stomata from 30 different plants for each group. (E) Local and systemic stomatal closure response of Arabidopsis mutants deficient in ABA biosynthesis (aba1-1, Ler; aba2-1 and aba3-1, Col) to local application of light stress. n = 500 stomata from 30 different plants for each group. (F) Local and systemic stomatal closure response of Arabidopsis mutants deficient in ABA sensing (abi1-1, Ler) to local application of light stress. n = 500 stomata from 30 different plants for each group. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE, *P < 0.05, ***P < 0.001. dw, dry weight.

  • Fig. 5 ABA is required for H2O2 and SA accumulation in local and systemic leaves of Arabidopsis plants subjected to local application of light stress.

    (A to D) Accumulation of ABA (A, n = 30 plants for each group), H2O2 (B, n = 30 plants for each group), jasmonic acid (JA) (C, n = 30 plants for each group), and salicylic acid (SA) (D, n = 30 plants for each group) in local and systemic leaves of wild-type Ler, aba1-1, and abi1-1 plants in response to local application of light stress. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE, ***P < 0.001, **P < 0.01, *P < 0.05.

  • Fig. 6 Transient accumulation of ABA, OPDA, and JA in local and systemic leaves of Arabidopsis plants subjected to local application of light stress, and a role for SLAC1, LOX1, and GHR1 in the local and/or systemic stomatal closure response of Arabidopsis to light stress.

    (A) Changes in the level of ABA in local (left) and systemic (right) leaves of wild-type (Col; top) and rbohD mutants (rbohD; bottom). n = 20 plants for each group (B) and (C), similar to (A), however, showing changes in 12-oxophytodienoic acid (OPDA) (B) and JA (C). n = 20 plants for each group (D) and (E). Impaired local and systemic stomatal closure response of Arabidopsis slac1 (D) and ghr1 (E) mutants (Col background) to local application of light stress. n = 500 stomata from 30 different plants in each group. (F) Impaired systemic, but not local, stomatal closure response of Arabidopsis lox1 mutants to local application of light stress. n = 500 stomata from 30 different plants for each group. Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE, ***P < 0.005, **P < 0.01, and *P < 0.05.

  • Fig. 7 Enhanced acclimation of systemic leaves is dependent on leaf-to-leaf rapid signaling, and a model for the interplay between ABA, ROS, and JA during rapid systemic stomatal responses of Arabidopsis to light stress.

    (A and B) Enhanced acclimation of systemic leaves to light stress. Plants were pretreated for 10 min with light stress on a local leaf (pretreated). Control plants were untreated (control). After 15 min, the systemic leaves of the treated or untreated plants were subjected to light stress (light stress) for 60 min and sampled for ion leakage measurements and imaging. Control plants were not given the 60-min light stress (no stress). Water (A) or DPI (50 μM) (B) was applied in agar at the midpoint between the local and systemic leaves (as in Fig. 2A). Statistical significance was determined by a one- or two-tailed Student’s t test as described in (25). Results are presented as the means ± SE (for each time point n = 30 different plants in each group), **P < 0.01, *P < 0.05. (C) A proposed model for the rapid systemic stomatal closure response of Arabidopsis to local application of light stress. The triggering of stomatal responses, accumulation of SA and H2O2, and the initiation of the ROS/Ca2+ wave in local leaves requires ABA. The closure of stomata in systemic leaves requires the ROS/Ca2+ wave and an interplay between JA, ABA, and ROS. The stomatal responses of both systemic and local leaves require GHR1 and SLAC1. Solid arrows represent tested interactions, and dashed arrows represent hypothetical interactions that require further studies.

Supplementary Materials

  • www.sciencesignaling.org/cgi/content/full/11/518/eaam9514/DC1

    Fig. S1. The light stress–induced stomatal closure response of Arabidopsis.

    Fig. S2. An increase in leaf temperature accompanies the stomatal closure response of local and systemic leaves to light stress applied to the local leaf.

    Fig. S3. ABA application to a local leaf triggers the ROS wave in local and systemic leaves.

    Fig. S4. Leaf temperature measurements of wild-type Ler and aba1-1 and abi1-1 mutants subjected to light stress applied to the local leaf.

    Fig. S5. Transient accumulation of SA in local and systemic leaves of Arabidopsis plants subjected to local application of light stress.

  • Supplementary Materials for:

    Coordinating the overall stomatal response of plants: Rapid leaf-to-leaf communication during light stress

    Amith R. Devireddy, Sara I. Zandalinas, Aurelio Gómez-Cadenas, Eduardo Blumwald, Ron Mittler*

    *Corresponding author. Email: ron.mittler{at}unt.edu

    This PDF file includes:

    • Fig. S1. The light stress–induced stomatal closure response of Arabidopsis.
    • Fig. S2. An increase in leaf temperature accompanies the stomatal closure response of local and systemic leaves to light stress applied to the local leaf.
    • Fig. S3. ABA application to a local leaf triggers the ROS wave in local and systemic leaves.
    • Fig. S4. Leaf temperature measurements of wild-type Ler and aba1-1 and abi1-1 mutants subjected to light stress applied to the local leaf.
    • Fig. S5. Transient accumulation of SA in local and systemic leaves of Arabidopsis plants subjected to local application of light stress.

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    © 2018 American Association for the Advancement of Science

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