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. 2019 Jul 26:17:144-154.
doi: 10.1016/j.isci.2019.06.024. Epub 2019 Jun 20.

Strigolactones Play an Important Role in Shaping Exodermal Morphology via a KAI2-Dependent Pathway

Guowei Liu  1 , Marina Stirnemann  1 , Christian Gübeli  1 , Susanne Egloff  1 , Pierre-Emmanuel Courty  2 , Sylvain Aubry  1 , Michiel Vandenbussche  3 , Patrice Morel  3 , Didier Reinhardt  4 , Enrico Martinoia  5 , Lorenzo Borghi  6
Affiliations

Strigolactones Play an Important Role in Shaping Exodermal Morphology via a KAI2-Dependent Pathway

Guowei Liu et al. iScience. .

Abstract

The majority of land plants have two suberized root barriers: the endodermis and the hypodermis (exodermis). Both barriers bear non-suberized passage cells that are thought to regulate water and nutrient exchange between the root and the soil. We learned a lot about endodermal passage cells, whereas our knowledge on hypodermal passage cells (HPCs) is still very scarce. Here we report on factors regulating the HPC number in Petunia roots. Strigolactones exhibit a positive effect, whereas supply of abscisic acid (ABA), ethylene, and auxin result in a strong reduction of the HPC number. Unexpectedly the strigolactone signaling mutant d14/dad2 showed significantly higher HPC numbers than the wild-type. In contrast, its mutant counterpart max2 of the heterodimeric receptor DAD2/MAX2 displayed a significant decrease in HPC number. A mutation in the Petunia karrikin sensor KAI2 exhibits drastically decreased HPC amounts, supporting the hypothesis that the dimeric KAI2/MAX2 receptor is central in determining the HPC number.

Keywords: Biological Sciences; Molecular Plant Pathology; Plant Biology; Plant Physiology.

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Conflict of interest statement

The authors declare no competing interest.

Figures

None
Graphical abstract
Figure 1
Figure 1
Effect of Strigolactones (SL) on Hypodermal Passage Cell Density (A–I) Trypan-blue-stained HPCs. Top view on the epidermal layer (A), hypodermis (B), inner cortex layer one (C), inner cortex layer two (D), and stele (E). Root tip from primary root (F), differentiated cells in root segment 7 cm above the root tip (G), representative HPCs in WT (H), and in dad1 (I). (J and K) HPC density in the SL transporter mutant pdr1 and in the SL biosynthesis mutant dad1; the density of HPCs in the SL biosynthesis mutant dad1 can be restored by exogenous 10 μM GR24. (L and M) HPC density dynamics in primary and lateral roots of V26 and dad1 mutant. HPC density was quantified in 2-, 3-, 4-, 5-, and 6-week-old seedlings. Stars above the bars indicate statistically significant difference (t test, *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001). For clear view of data, scales in Figures 1J–1M are different. Scale bar, 50 μM (A–E, H, and I) and 250 μM (F and G). Error bars are ±SEM.
Figure 2
Figure 2
Exogenous Hormonal Treatments Affect HPCs Density (A) Effect of 1 μM ABA on HPC density. (B) Effect of ethylene on HPC density (1 μM ethephone or 5 μM ACC). (C) Effect of 1 μM Auxin (NAA) and 10 μM AVG on HPC density. (D) Free auxin content in WT and 35S:IaaL lines expressed relative to both fresh weight (FW) and dry weight (DW). (E) HPC densities in Petunia plants transgenic for the over-expression of the auxin-lysine conjugation enzyme (35S:IaaL). (F) HPC density in V26 and DAD1-OE roots. (G) HPC distribution in WT and DAD1-OE lines. (H) DAD1 expression in WT and DAD1-OE lines. (I) Arbuscular mycorrhizal (AM) structures quantified in WT and DAD1-OE roots 1 month after inoculation (m.a.i.) with Rhizophagus irregularis: hyphae, intraradical arbuscules, and vesicles. Negative means no AM structure detected. (J) Mycorrhization rates in W115 and DAD1-OE. Different letters above the bars indicate statistically significant difference (p < 0.05, by one-way ANOVA, n ≥ 30). Stars above the bars indicate statistically significant difference (t test, *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001, ****p ≤ 0.0001). Error bars are ±SEM. See Table S1.
Figure 3
Figure 3
Presence of HPCs is MAX2-Dependent and DAD2-Independent (A) HPC density in dad2 and WT roots. (B) DAD1 expression in dad2 mutant. (C) Mycorrhization ratios in V26 and dad2 mutant. (D) HPC density in max2a. (E) DAD1 and MAX1 gene expression levels in max2a. (F) HPC density in kai2a. Different letters above the bars indicate statistically significant difference (p < 0.05, by one-way ANOVA, n ≥ 30). Stars above the bars indicate statistically significant difference (t test, *p ≤ 0.05, **p ≤ 0.01, ***p ≤ 0.001, ****p ≤ 0.0001). Error bars are ±SEM. See Table S1.
Figure 4
Figure 4
Effects of GR24 Enantiomers and Karrikins on HPCs (A) HPC density after 1 μM karrikin1 and 1 μM karrikin2 treatments. (B) HPC density in WT and kai2a after treatments with 1 μM GR24 enantiomers. (C) HPCs in dad1 after treatments with mock, 1 μM, and 100 nM GR245DS. (D) Model of HPC regulation via SL5DS. Different letters above the bars indicate statistically significant difference (p < 0.05, by one-way ANOVA, n ≥ 30). When no letters, no significant difference. Stars above the bars indicate statistically significant difference (Student's t test p value < 0.05 = *; <0.001 = **). Error bars are ±SEM. See Table S1.
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