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. 2020 Jul 16;20(1):335.
doi: 10.1186/s12870-020-02544-8.

Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon

Bo Eun Nam  1   2 , Young-Joon Park  1 , Kyung-Eun Gil  1 , Ju-Heon Kim  1 , Jae Geun Kim  2 , Chung-Mo Park  3   4
Affiliations

Auxin mediates the touch-induced mechanical stimulation of adventitious root formation under windy conditions in Brachypodium distachyon

Bo Eun Nam et al. BMC Plant Biol. .

Abstract

Background: It is widely perceived that mechanical or thigmomorphogenic stimuli, such as rubbing and bending by passing animals, wind, raindrop, and flooding, broadly influence plant growth and developmental patterning. In particular, wind-driven mechanical stimulation is known to induce the incidence of radial expansion and shorter and stockier statue. Wind stimulation also affects the adaptive propagation of the root system in various plant species. However, it is unknown how plants sense and transmit the wind-derived mechanical signals to launch appropriate responses, leading to the wind-adaptive root growth.

Results: Here, we found that Brachypodium distachyon, a model grass widely used for studies on bioenergy crops and cereals, efficiently adapts to wind-mediated lodging stress by forming adventitious roots (ARs) from nonroot tissues. Experimental dissection of wind stimuli revealed that not bending of the mesocotyls but physical contact of the leaf nodes with soil particles triggers the transcriptional induction of a group of potential auxin-responsive genes encoding WUSCHEL RELATED HOMEOBOX and LATERAL ORGAN BOUNDARIES DOMAIN transcription factors, which are likely to be involved in the induction of AR formation.

Conclusions: Our findings would contribute to further understanding molecular mechanisms governing the initiation and development of ARs, which will be applicable to crop agriculture in extreme wind climates.

Keywords: Adventitious root; Auxin; Brachypodium distachyon; Gravity; Lodging; Thigmomorphogenesis; Wind.

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Conflict of interest statement

The authors declare that they have no competing interests.

Figures

Fig. 1
Fig. 1
Adaptation of Brachypodium plants to wind-induced mechanical stimulation. Three-week-old plants grown in soil were either exposed to a constant unidirectional wind flow or grown under control conditions (no wind) for 10 days and then subjected to wind treatments (wind-acclimated or nonacclimated, respectively). a Lodging phenotypes in response to wind stimulation were analyzed by measuring the angles of lodged tillers relative to the soil surface (θ). b Wind-treated plants were photographed, and the largest angles were measured. Box plots show the range of the angles of lodged tillers (n > 20). Different letters represent a significant difference (P < 0.01) determined by the Tukey’s honestly significant difference (HSD) test
Fig. 2
Fig. 2
Induction of AR formation by wind stimulation. Three-week-old plants were either exposed to a unidirectional wind flow or grown under mock conditions (no wind) for 10 days prior to analyzing AR emergence. a AR emergence. ARs formed in the soil-grown plants and their enlarged views were displayed (left photographs). White arrows indicate ARs. Leaf node roots formed on the tillers were counted as ARs. Three independent experiments, each consisting of 16 plants, were statistically analyzed (t-test, *P < 0.01) (right graph). Error bars indicate standard error of the mean (SE). b Wind response of plants with or without ARs. Visible ARs of the unidirectional wind-treated plants were either retained (no cut) or cut out, and the plants were exposed to wind stimulation (left photographs). The angles of lodged tillers were statistically analyzed (right graph, n = 20). Different letters represent a significant difference (P < 0.01) determined by the Tukey’s HSD test
Fig. 3
Fig. 3
Effects of wind-driven falling down on AR formation. Three-week-old plants grown in soil were further grown for 10 days under various experimental conditions. Three independent experiments, each consisting of 16 plants, were statistically analyzed (t-test, *P < 0.01). Error bars indicate SE. White arrows indicate ARs. a Induction of AR formation by wind-induced lodging. Plants were exposed to wind flow with or without supporting wires, which protect plants from falling down. Following wind treatments, representative plants were photographed (left photographs), and AR emergence was statistically analyzed (right graph). b Effects of mechanical and gravity stimuli. Plants were artificially fallen down using wires (fallen). Plants were also grown on a slope of 75o to impose gravity stimulation (rotated). Following treatments, representative plants were photographed (left photographs), and AR emergence was statistically analyzed (right graph). c Effects of a combined stimulation of falling down and gravity. Plants were artificially fallen down and then rotated by 75o to impose a combined stimulation. Representative plants were photographed (left photographs), and AR emergence was statistically analyzed (right graph)
Fig. 4
Fig. 4
Induction of AR formation by physical soil contact. Three independent experiments, each consisting of 16 plants, were statistically analyzed using Student t-test (*P < 0.01). Error bars indicate SE. a Stimulation of AR formation by soil contact. Plants were artificially fallen down, as described in Fig. 3b. The leaf nodes of the fallen plants were then embedded in the soil for 10 days. Representative plants were photographed (left photographs). Arrows and arrowheads indicate ARs formed at the lower and upper sides of the fallen tillers, respectively. Asterisks mark AR primordia. AR emergence was statistically analyzed (right graph). b Induction of AR formation by sand-driven mechanical touch. Leaf nodes were covered with soil or sand stack (left photographs). To minimize the sand humidity, miracloth was put in between the soil and sand stacks (sand+paper). AR emergence was statistically analyzed (right graph)
Fig. 5
Fig. 5
Auxin-mediated induction of AR formation. To examine the effects of growth hormone inhibitors on AR formation, three-week-old plants grown in soil were artificially fallen down, and the NPA or AgNO3 solution (1 μM each) was sprayed once a day for 10 days. a Representative plants were photographed. Arrows indicate ARs. AR emergence (b) and number of ARs per plant (c) were analyzed. Three independent experiments, each consisting of 16 plants, were statistically analyzed (t-test, *P < 0.01). Error bars indicate SE
Fig. 6
Fig. 6
Auxin-mediated stimulation of WOX and LBD gene expression in artificially fallen plants. The phylogenetic trees were generated using the Neighbor-Joining method of the MEGA7 software (https://www.megasoftware.net) (a, b). In the phylogenetic analysis, protein members that have been functionally characterized were marked in bold. For gene expression analysis, three-week-old plants grown in soil were sprayed with either 0.1 mM IAA or 1 μM NPA solution and then artificially fallen down to the soil surface (c, d). The first leaf nodes and their internodes were harvested at the indicated time points for the extraction of total RNA samples. Transcript levels were analyzed by RT-qPCR. Biological triplicates, each consisting of 15 plants, were statistically analyzed. Error bars indicate SE. a Phylogenetic analysis of Brachypodium WOX proteins. b Effects of auxin and NPA on the transcription of Brachypodium WOX genes. c Phylogenetic analysis of Brachypodium LBD proteins. d Effects of auxin and NPA on the transcription of LBD genes
Fig. 7
Fig. 7
Induction of WOX and LBD genes by wind-mediated mechanical stimulation. Following stimulation by wind and artificial falling down, the first leaf nodes and their internodes were harvested for total RNA extraction, and transcript levels were analyzed by RT-qPCR. Biological triplicates, each consisting of 15 plants, were statistically analyzed (t-test, *P < 0.01). Error bars indicate SE. a, b Transcription of WOX and LBD genes. Three-week-old plants grown in soil were exposed to either a constant wind flow (a) or artificially fallen down (b) for 6 h. c, d Transcription of ethylene response genes. The plants treated with either wind flow (c) or falling down (d) for 6 h were used. e Schematic model of auxin-mediated AR formation under wind-induced lodging stress conditions. In response to wind flow, plants falls down, imposing a mechanical stimuli on the leaf nodes. The mechanical stimulation would induce the auxin-dependent expression of WOX and LBD genes. We propose that the WOX/LBD-mediated auxin signals trigger the initiation and development of ARs, leading to plant adaptation to lodging stress
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