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Expression of MAX2 under SCARECROW promoter enhances the strigolactone/MAX2 dependent response of Arabidopsis roots to low-phosphate conditions

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Abstract

Main conclusion

MAX2/strigolactone signaling in the endodermis and/or quiescent center of the root is partially sufficient to exert changes in F-actin density and cellular trafficking in the root epidermis, and alter gene expression during plant response to low Pi conditions.

Strigolactones (SLs) are a new group of plant hormones that regulate different developmental processes in the plant via MAX2, an F-box protein that interacts with their receptor. SLs and MAX2 are necessary for the marked increase in root-hair (RH) density in seedlings under conditions of phosphate (Pi) deprivation. This marked elevation was associated with an active reduction in actin-filament density and endosomal movement in root epidermal cells. Also, expression of MAX2 under the SCARECROW (SCR) promoter was sufficient to confer SL sensitivity in roots, suggesting that SL signaling pathways act through a root-specific, yet non-cell-autonomous regulatory mode of action. Here we show evidence for a non-cell autonomous signaling of SL/MAX2, originating from the root endodermis, and necessary for seedling response to conditions of Pi deprivation. SCR-derived expression of MAX2 in max2-1 mutant background promoted the root low Pi response, whereas supplementation of the synthetic SL GR24 to these SCR:MAX2 expressing lines further enhanced this response. Moreover, the SCR:MAX2 expression led to changes in actin density and endosome movement in epidermal cells and in TIR1 and PHO2 gene expression. These results demonstrate that MAX2 signaling in the endodermis and/or quiescent center is partially sufficient to exert changes in F-actin density and cellular trafficking in the epidermis, and alter gene expression under low Pi conditions.

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Abbreviations

(+)-GR24:

(3aR,8bS,2′R)-GR24

APL:

Altered phloem development

MAX2:

More axilary growth2

hpg:

Hours post-germination

NST3 :

NAC secondary wall thickening promoting factor3

Pi:

Inorganic phosphate

PSI:

Phosphate-starvation induced genes

RH:

Root hair

SCR:

SCARECROW

SLs:

Strigolactones

WOX4 :

Wuschel-related homeobox4

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Acknowledgments

OM is supported by a scholarship from The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, Ramat-Gan, Israel. This article is based upon work from COST Action (FA1206), supported by COST (European Cooperation in Science and Technology).

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Authors and Affiliations

  1. Institute of Plant Sciences, Agricultural Research Organization (ARO), The Volcani Center, 50250, Bet Dagan, Israel

    Ortal Madmon, Moran Mazuz, Puja Kumari, Anandamoy Dam, Aurel Ion, Einav Mayzlish-Gati, Eduard Belausov, Smadar Wininger, Mohamad Abu-Abied, Yoram Kapulnik & Hinanit Koltai

  2. The Mina and Everard Goodman Faculty of Life Sciences, Bar-Ilan University, 52900, Ramat-Gan, Israel

    Ortal Madmon & Rafael Perl-Treves

  3. School of Chemistry, The University of Sydney, Sydney, NSW, 2006, Australia

    Christopher S. P. McErlean & Liam J. Bromhead

  4. Dipartimento di Chimica, Turin University, 10125, Turin, Italy

    Cristina Prandi

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  1. Ortal Madmon
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  2. Moran Mazuz
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Electronic supplementary material

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Supplementary material 1

Root-hair (RH) density (RH /1000μm) under high phosphate (Pi) conditions at 48 hpg of wild type (WT; Col-0), max2-1, max4-1 and lines expressing MORE AXILLARY GROWTH 2 (MAX2) under different tissue-specific promoters in max2-1 mutants, including SCR:MAX2 (40-5 and 90-1), NST3:MAX2 (73-2 and 39-2), APL:MAX2 (37-3 and 37-1) and WOX4:MAX2 (89-3 and 92-2; Agusti et al. 2011).SCR, SCARECROW; NST3, NAC SECONDARY WALL THICKENING PROMOTING FACTOR3; APL, ALTERED PHLOEM DEVELOPMENT; WOX4, WUSCHEL-RELATED HOMEOBOX4. Means ± SE are shown; n=60. No significant differences were detected between means by one-way analysis of variance (ANOVA) with Tukey–Kramer multiple comparison test (P< 0.01) (DOCX 13 kb)

Supplementary material 2

Effect of low phosphate (Pi) conditions and exogenous supplementation of GR24 on root-hair (RH) density (RH /1000μm) at 48 hpg of wild type (WT; Col-0), max2-1, max4-1 and lines expressing MORE AXILLARY GROWTH 2 (MAX2) under different tissue-specific promoters in max2-1 mutants, including SCR:MAX2 (40-5 and 90-1), NST3:MAX2 (73-2 and 39-2), APL:MAX2 (37-3 and 37-1) and WOX4:MAX2 (89-3 and 92-2; Agusti et al. 2011) (SCR, SCARECROW; NST3, NAC SECONDARY WALL THICKENING PROMOTING FACTOR3; APL, ALTERED PHLOEM DEVELOPMENT; WOX4, WUSCHEL-RELATED HOMEOBOX4). Grey bars, (±)-GR24-treated; Black bars, acetone (AC) control. Means ± SE are shown; n=60. Different letters above bars indicate statistically significant differences between means by one-way analysis of variance (ANOVA) with Tukey–Kramer multiple comparison test (P ≤ 0.05). Two-way ANOVA analysis revealed significance between treatments and Arabidopsis lines (P< 0.001) (PDF 244 kb)

Supplementary material 3

Examples for TALIN–GFP F-actin in the epidermal cells of the primary root elongation zone in 35S:TALIN–GFP roots of seedling grown under high (2 mM) and low (1 μM) Pi conditions (48 hpg). TALIN–GFP signal in Col-0 or max2-1 mutant (max2-1–28) or 40-5-10 line expressing MAX2 under the SCR tissue-specific promoter in max2-1 mutant, grown under high- or low-Pi conditions. Bars, 20 μm (PDF 250 kb)

Supplementary material 4

Examples for TALIN–GFP F-actin in the epidermal cells of the primary root elongation zone in 35S:TALIN–GFP roots of seedling grown under low (1 μM) Pi conditions (48 hpg), acetone control (AC) or with the addition of (+)-GR24 ((3aR,8bS,2′R)-GR24). TALIN–GFP signal in Col-0 or max2-1 mutant (max2-1–28) or 40-5-10 line expressing MAX2 under the SCR tissue-specific promoter in max2-1 mutant, grown under low-Pi conditions. Bars, 20 μm (PDF 529 kb)

Supplementary material 5

Examples for endosomal movement in the epidermal cells of the primary-root elongation zone in 35S:ARA7–GFP seedlings grown under high (2 mM) and low (1 μM) Pi conditions (48 hpg). ARA7–GFP signal in Col-0 or max2-1 mutant (max2-1–73) or 40-5-8 line expressing MAX2 under the SCR tissue-specific promoter in max2-1 mutant. Overlay of frame 1(green) on frame 5(+16 s, red), and on frame 9 (+29 s, blue) of ARA7. Bars, 10 μm (PDF 462 kb)

Supplementary material 6

Examples for endosomal movement in the epidermal cells of the primary-root elongation zone in 35S:ARA7–GFP seedlings grown under low (1 μM) Pi conditions (48 hpg), acetone control (AC) or with the addition of (+)-GR24 ((3aR,8bS,2′R)-GR24). ARA7–GFP signal in Col-0 or max2-1 mutant (max2-1–73) or 40-5-8 line expressing MAX2 under the SCR tissue-specific promoter in max2-1 mutant, grown under low-Pi conditions. Overlay of frame 1(green) on frame 5(+16 s, red), and onframe 9 (+29 s, blue) of ARA7. Bars, 10 μm (PDF 462 kb)

Supplementary material 7 (PDF 473 kb)

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Madmon, O., Mazuz, M., Kumari, P. et al. Expression of MAX2 under SCARECROW promoter enhances the strigolactone/MAX2 dependent response of Arabidopsis roots to low-phosphate conditions. Planta 243, 1419–1427 (2016). https://doi.org/10.1007/s00425-016-2477-7

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