Two distinct oscillatory auxin signals define the plasticity of lateral rooting in Arabidopsis thaliana

doi:10.21203/rs.3.rs-4945759/v1

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Two distinct oscillatory auxin signals define the plasticity of lateral rooting in Arabidopsis thaliana

https://doi.org/10.21203/rs.3.rs-4945759/v1

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The so-called root clock defines lateral root pre-branch sites (PBS) but how these sites contribute to the root system architecture remains incompletely understood^1,2,3,4. Here we reveal in the model plant Arabidopsis thaliana that two distinct oscillatory systems for the phytohormone auxin coordinate the spatial and temporal identity of PBS, jointly defining the lateral root density. We followed auxin signalling dynamics for days and thereby detected a systemic auxin signal oscillating in the mature primary root, which is distinct from the previously described root clock at the root tip. While the root clock spatially primes the PBS in the growing root tip, the systemic oscillatory auxin signal temporally controls the auxin-dependent identity of these PBS. Light perception in the shoot defines the strength of the systemic auxin signal and thereby controls the auxin-reliant ability of PBS to develop into lateral roots. Moreover, PHYB and CRY1 mediate the light-dependent integration of other environmental signals, such as ambient temperature, into the control systemic auxin signalling and lateral root density. Our work reveals how two spatially distinct oscillatory auxin signals define the plasticity of plant root development in response to fluctuating conditions.

Biological sciences/Plant sciences/Plant hormones/Auxin

Biological sciences/Plant sciences/Plant development/Plant morphogenesis

Biological sciences/Plant sciences/Plant signalling

Biological sciences/Plant sciences/Plant stress responses/Abiotic

De novo organogenesis is a hallmark of the remarkable plasticity and adaptability in plants. In the context of root system architecture, lateral root (LR) formation is a critical process that enhances nutrient and water uptake, providing stability and resilience. The LR density is tightly controlled and the sites of presumptive LR development are predetermined along the primary root axis through a mechanism, which involves the so-called "root clock"^1,2,3. The root clock generates an oscillatory signal of the phytohormone auxin in the elongation zone of the main root, thereby marking the LR pre-branch sites (PBS)². While the root clock is established as a mechanism for generating PBS, there is controversy regarding whether these sites consistently mark the exact locations of LR development⁴. We used prolonged imaging of the synthetic, auxin-responsive DR5 promoter fused to a luciferase reporter (pDR5::Luc)² to visualize the nuclear auxin output signalling and therewith PBS dynamics for days at constant light (120 µmol·m^− 2·s^− 1) and temperature (21°C) conditions. Therewith, we revealed that indeed a substantial fraction of the PBS lost the auxin signal in time and did not give rise to LR development (Supplementary Fig. 1). We, hence, addressed the currently elusive mechanism that decisively defines the transient or persistent nature of the auxin-reliant PBS and its contribution to control LR density.

To analyze the long-term dynamics of DR5 luciferase activity, we utilize kymograph representations, which are graphical depictions of spatial position (top to bottom) over time (left to right), essentially capturing the dynamic changes along a segmented root in a single image. This approach allowed us to detect a systemic DR5 oscillatory behaviour along the entire primary root, including the PBS, being distinct from the spatially defined auxin oscillation zone of the root tip (Fig. 1a,b and Supplementary Fig. 2a). In our constant growth condition, the frequency of this systemic DR5 oscillatory behaviour followed a normal distribution (Anderson-Darling normality test, P-value = 0.4501) with a period of around 24 hours (Fig. 1c, Supplementary Fig. 2b). We subsequently assessed if environmental factors, such as light intensity affect this systemic oscillatory auxin signal. When compared to control 120 µmol·m^− 2·s^− 1 light conditions (hereafter referred to as high light, HL), a reduction of the light intensity to 50 µmol·m⁻²·s⁻¹ (hereafter referred to as medium light, ML) did not affect the frequency of the systemic auxin oscillations (Anderson-Darling normality test, P-value = 0.177) (Fig. 1d,e and Supplementary Fig. 2c,d) but did quantitatively decrease the overall intensity of the systemic auxin signal (Fig. 1f). Notably, the systemic nuclear auxin signalling was undetectable at a light intensity of 20 µmol·m⁻²·s⁻¹ (hereafter referred to as low light, LL) (Fig. 1g and Supplementary Fig. 3).

Based on these results, we propose that light quantitatively controls a systemic oscillatory auxin signal. Next, we addressed whether the systemic auxin signalling dynamics contribute to the transient nature of auxin-reliant PBS. Notably, despite the varying strength of systemic auxin signalling at different light intensities, we observed similar quantities of PBS under HL, ML, and LL conditions (Fig. 1h), indicating that the initial priming of PBS is largely independent of light intensity. However, we observed a correlation between the impediment of systemic auxin signalling and a steep increase in transient auxin signal in PBS at LL conditions (Fig. 1i). This result suggests that light intensity contributes to maintaining the auxin-reliant identity of PBS, correlating with a quantitative impact on systemic auxin oscillation.

To specifically address the light dependency of already formed PBS, we monitored PBS formation in 5-day-old pDR5::Luc seedlings under HL conditions for 48 hours and afterwards exposed them either to LL conditions or maintained them under HL as a control. After transferring seedlings from HL-to-LL conditions, the systemic auxin signalling completely ceased, observing the last oscillatory peak after 8 hours (Fig. 2a and Supplementary Fig. 4a). Additionally, although the total quantity of PBS was similar under both light conditions (Supplementary Fig. 5), the HL-to-LL transfer revealed that light intensity is critical to maintaining auxin signalling in PBS when compared to seedlings kept in HL (Fig. 2c,d). These findings confirm that light intensity is crucial to maintaining the systemic oscillatory auxin signal and PBS identity.

Contrariwise, we also monitored PBS formation in 5-day-old pDR5::Luc seedlings under LL conditions for 48 hours and subsequently transferred the seedlings either to HL conditions or kept them at LL as a control. In this condition, systemic auxin dynamics recovered around 18 hours after transferring from LL-to-HL (Fig. 2b and Supplementary Fig. 4b). Moreover, HL recovered auxin signalling in PBS when compared to those kept in LL (Fig. 2c,d). This finding again pinpoints the positive impact of light on systemic auxin signalling and its ability to reactivate auxin-reliant PBS.

Next, we tested if the light-dependent gating of auxin in PBS indeed contributes to the reshaping of the root system architecture. To ensure the light effects are independent of LR priming, we transferred 7-day-old seedlings between different light conditions and analyzed three days later the LR appearance in a defined section of the main root (grown between days 4 and 7; see marks in Fig. 2e). We observed a strong decrease in LR density when transferring roots from HL-to-LL compared to those maintained at HL (Fig. 2e,f). Conversely, LR density significantly increased when transferring from LL-to-HL as compared to those kept at LL (Fig. 2e,f). This set of data confirms that light conditions control auxin-dependent PBS and thereby LR density. Accordingly, we propose that light quantitatively controls systemic oscillatory auxin signals, thereby temporally gating the identity of previously primed PBS and ultimately LR spacing.

Based on our data we hypothesize that a local auxin oscillation zone (root clock) enables the regular priming of PBS during main root growth, whereas a systemic oscillatory auxin signal could integrate various environmental information into lateral root spacing. To further test this assumption, we introduced variation in ambient temperature. Temperature and light signalling both play a crucial role in shaping root system architecture and are in part molecularly interconnected⁵. However, the current literature presents conflicting findings, indicating that increased ambient temperature can have both stimulative and inhibitory effects on lateral rooting within and across different species^{6,7,8,9,10,11,12}. To shed light on this seemingly complex role, we initially tested whether temperature also affects auxin signalling dynamics in the root, we transferred 5-day-old pDR5::Luc seedlings from a controlled temperature of 21°C to a high ambient temperature (HT) of 29°C at constant HL condition. By monitoring the root luminescence after the transfer, we observed an overall increase of auxin signalling in the focal oscillation (root clock) zone (Fig. 3a,b), which also correlates with an increased number of PBS (Fig. 3c). However, the vast majority of auxin-reliant PBS appeared transiently, being reflected in time by a severe systemic disruption of auxin signalling (Fig. 3d,e and Supplementary Fig. 6). Our results suggest that HT imposes initially a positive effect on initiating PBS but subsequently a negative effect on the systemic auxin signal along the primary root. Contrary to this observation, the lateral root primordia (LRP) (Supplementary Fig. 7) and overall LR density (Fig. 3f,g) were not inhibited by HT but showed even slight enhancement when compared to the control.

To further address this paradox, we extended our imaging of the auxin output signalling to 8 days. Thereby, we observed a recovery of the systemic auxin signalling along the entire root around 70 hours after transferring seedlings to HT conditions (Fig. 3h and Supplementary Fig. 8). The systemic peak in auxin correlates with the reactivation of PBS, ultimately resulting in an increase in persistent PBS at HT (Fig. 3h,i). Notably, the number of recovered, persistent PBS under this condition is remarkably similar to the number in the control temperature condition (Fig. 3i). The reactivation of PBS strictly occurs simultaneously or after recovery of systemic auxin peak (Fig. 3h, Supplementary Fig. 8), suggesting again that a systemic auxin signal enables the environmental control of already primed PBS.

To confirm that the systemic auxin signal indeed integrates environment information into lateral rooting, we quantitatively lowered the HT-induced recovery of the systemic auxin signal, using medium light conditions. Accordingly, we grew pDR5::Luc seedlings at 21°C and ML and transferred 5-day-old seedlings to HT and ML conditions. Similar to seedlings at HL (Fig. 3), HT also increased the auxin signalling output at the focal oscillatory zone (Fig. 4a,b), correlating with initially enhanced PBS priming at ML conditions when compared to the control (Fig. 4c). Similar to the HL condition, the formed PBS showed transient auxin signals, being reflected by a strong, systemic disruption of auxin signalling in the mature root.

The HT also induced a temporal decline (Fig. 4d,e and Supplementary Fig. 9) and systemic recovery of auxin signalling in ML conditions, but, importantly, the recovery of the systemic signal was as anticipated quantitatively reduced (Fig. 4h) when compared to HL conditions. Notably, the systemic auxin recovery was also temporarily delayed, occurring around 100 hours after the transfer (Fig. 4f,g and Supplementary Fig. 10). In agreement with our assumptions, ML-dependent reduction in systemic auxin signal also reduced the recovery of auxin-reliant PBS (Fig. 4i) when compared to HL conditions. This set of data confirms that light-dependent, systemic oscillatory auxin signalling defines the transient or persistent nature of PBS. Moreover, our data suggests that light quantity gates the negative impact of HT on PBS progression.

We next tested whether the proposed light-dependent gating of ambient temperature indeed defines root system architecture. In contrast to the limiting effect of HT on LR density under HL conditions (Fig. 3), HT induced a strong reduction in the density under ML conditions (Fig. 4j,k), confirming that light quantity indeed contextualizes the integration of ambient temperature into root system architecture.

Next, we tested if this gating mechanism defines not only PBS identity but also blocks the LRP development. Whereas the LR density was decreased in these conditions, it did not increase the number of non-emerged lateral roots but showed a quantitively similar amount of LRP when compared to the control condition (Supplementary Fig. 11). This finding suggests that light-gated HT response does not primarily block LRP progression but impacts on PBS identity. In agreement with its impediment in systemic auxin signalling, we observed that the HT-dependent inhibition of lateral rooting was further enhanced under LL conditions (Supplementary Fig. 12). This set of data indicates that systemic oscillation of auxin integrates environmental signals, such as light and temperature, into the temporal control of PBS, contributing significantly to the root system architecture. We hence propose that the effect of high ambient temperature on lateral rooting is conditional, which can explain the seemingly conflicting literature on high temperature and its impact on lateral rooting^{6,7,8,9,10,11,12}.

Besides its impact on lateral rooting, high temperature also enhances main root growth in an auxin-dependent manner^13,14,15. It has been proposed that the priming of lateral roots may depend on the interplay of auxin and main root growth dynamics^16,17. Therefore, we next aimed to address whether HT-induced main root growth is linked to lateral rooting under our conditions. HT induced main root growth in HL, but this effect was abolished in ML conditions, which is conversely to its impact on lateral rooting (Supplementary Fig. 13a,b). These findings indicate that HT affects lateral rooting and main root growth via distinct mechanisms.

Next, we used light exposure of the root or shoot only to dissect where the light signal that modulates lateral rooting is perceived. We found that light exposure of the shoot is not only essential for lateral root development but also sufficient to gate the temperature-dependent lateral rooting (Supplementary Fig. 14a-f). Hence, we assume that light perception in the shoot contributes to the auxin-reliant lateral rooting mechanism. Subsequently, we investigated the genetic mechanism of light-gated HT-dependent repression of lateral rooting. Mutations in the phytochrome B (phyB) red and far-red light photoreceptor caused hypersensitivity to HT-induced repression of lateral rooting at ML conditions when quantitatively compared to the wild-type (Supplementary Fig. 15a-c). In addition to functioning as a light sensor, PHYB also acts as a thermosensor¹⁸. However, the increased hypersensitivity to HT-induced repression of lateral rooting observed in the phyB-9 mutant suggests that PHYB does not function as the thermosensor in this process (Supplementary Fig. 15a-c). Moreover, we detected a similar hypersensitivity to HT at ML condition in mutants of the blue light receptor cryptochrome 1 (CRY1) (Supplementary Fig. 15a-c). Notably, triple mutants of phyBcry1cry2 not only enhanced hypersensitivity to HT-induced repression of lateral rooting at ML conditions compared to single mutants of phyB-9 and cry1-304 (Supplementary Fig. 15a-c), but also caused sensitivity to HT at HL conditions when compared to the wild-type, which was not observed in the single mutant of phyB-9 and cry1-304 (Fig. 4l-n). In contrast, the genetic interference with phytochrome A (phyA) or phototropins (PHOTs) had no major impact on the high-temperature-induced repression of lateral root development (Supplementary Fig. 16a-e). We accordingly conclude that PHYB and CRY1 jointly mediate the light-gated integration of ambient temperature into the root system architecture.

PHYB and CRY1 both mediate light signals by regulating PHYTOCHROME INTERACTING FACTORS (PIFs) and ELONGATED HYPOCOTYL5 (HY5) module, which is also known to integrate light quality during the shade avoidance response into the rate of lateral rooting^19,20,21. However, neither the quadruple mutant pif1,3,4,5 (pifQ), nor hy5-215 mutant was distinguishable from the wild type in regards to HT-dependent lateral rooting under ML condition (Supplementary Fig. 16a and f-i). This suggests a molecularly distinct mechanism for the integration of light quality during shade avoidance and the light quantity-dependent gating of HT into lateral rooting.

Mechanistically, we reveal that the perception of light quantity in the shoot defines the strength of a systemic oscillatory auxin signal in the main root, thereby defining the auxin-dependent identity of lateral root PBS. The light-dependent, systemic auxin dynamics also gate HT-dependent control of PBS progression to lateral roots, suggesting a general mechanism for environmental signal integration. Conceptually, our work illustrates that two oscillatory systems define LR spacing. While a local auxin oscillation zone (root clock) regulates the regular priming of PBS during main root growth, the systemic oscillatory auxin signal along the main root integrates environmental information, such as light and temperature, to control the PBS identity in time and eventually its progression to become lateral roots. This framework reveals how plants mechanistically use two oscillatory signals of the same regulator to combine robustness and plasticity into de novo organogenesis.

Acknowledgements: We thank Stefan Kircher and Andreas Hiltbrunner for providing seed materials and critically reviewing the manuscript; Stefan Kircher for assistance with root luminescence imaging and analysis; Deutsche Forschungsgemeinschaft (DFG) (DFG; 470007283 to J.K.-V. and CIBSS – EXC-2189; 390939984 to J.K.-V.) and Chinese Scholarship Council (CSC, 202006300036 to C.R.) for funding.

Author contributions: C.R. and J.K.-V. designed the research; C.R. and J.B. performed the research; C.R. analyzed data; and C.R. and J.K.-V. wrote the paper.

Competing interests: The authors declare no competing interests.

Additional Information: Correspondence and requests for materials should be addressed to J.K.-V ([email protected]).

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Plant Materials

The Arabidopsis thaliana ecotype Columbia 0 (Col-0) and Landsberg (Ler) were used as the wild type in this study. The pDR5:Luc² is in the ecotype Col-0 accession and was received from Stefan Kircher. The mutants of phyA-211²², phyB-9²³, cry1-304²⁴, pif1,3,4,5²⁵ and hy5-215²⁶ mutants are all in the Col-0 accession and were received from Andreas Hiltbrunner. The mutant of phyBcry1cry2²⁷ is in the ecotype Ler accession and was received from Stefan Kircher.

Growth conditions and treatments

The Arabidopsis seeds were sterilized for 2–5 minutes with 70% ethanol, followed by drying. After sterilization, the seeds were uniformly plated on one single line on square plates (12 × 12 × 1.5 cm). The plates contained 50 mL standard Murashige and Skoog solid medium, which is made of 0.8% agar, 0.5× Murashige and Skoog (MS) medium, and with 1% sucrose (MS+, no exogenous sucrose was added for MS-) (pH 5.9). Subsequently, the seeds were stratified for 2 days in 10 °C and dark conditions. Seeds were germinated on vertically positioned plates within a Weiss-Technik incubator (Fitotron SGC 2), exposed to top-providing illumination from LED white cultivation lights (16h day/8h night cycle) in 21 ºC and an irradiance of 120 µmol m⁻² s⁻¹. Plates grow under the above control condition for 4 days (root quantification assay) or 5 days (luminescence monitoring assay) before subsequent experiments. For light conditions and HT treatment, two Weiss-Technik incubators were configured at either 21°C (control) or 29°C (HT), operating under constant light. Each incubator was outfitted with top LED white culture lights arranged across three distinct culture levels, featuring irradiances of 20, 50, and 120 (control) µmol m⁻² s^-1.

Root quantification

For root phenotyping, surface-sterilized seeds were uniformly plated, stratified, and germinated on a square plate (12 × 12 × 1.5 cm) as described above. After germination under the control condition for 4 days, marking the position of the root tip, the 4-day-old seedlings were then transferred to the treatment condition (either 21°C or 29°C with light conditions set at 20, 50 or 120 µmol m⁻² s^-1) for additional 3 days and the root tip positions were marked again. For lateral and primary root phenotyping, the plates were scanned at 600 dpi using an Epson V850Pro photonegative scanner at 24-hour intervals, starting from the 3rd day to the 10th day of treatments. The lateral roots between the two marked root section were counted manually from the images and the length of primary roots between two marked positions was measured automatically using the SNT plugin or manually with Fiji/ImageJ. The significance test was conducted in R using the t.test and aov functions.

Lateral root primordia quantification

To phenotype lateral root primordia, seeds were placed on individual square plates. After marking the root tips of 4-day-old seedlings, they were moved to specific treatment conditions as outlined in the manuscript and figure legend (either 21°C or 29°C with light conditions set at 50 or 120 µmol m⁻² s^-1). Following a 3-day treatment, the positions of the root tips were marked again, and the plates were scanned to measure the length of the primary roots. After 5 days of treatment, primary roots located between two marked positions were harvested, followed by fixation and clearing in accordance with a previously published protocol²⁸. The roots were mounted in 50% glycerol and analyzed using a Zeiss AxioObserver Z1 microscope (Plan-Apochromat 40×/0.95 objective) with a AxioCam MRc camera. Primordia were counted manually, and the length of primary roots between two marked positions was determined as described above. The significance test was conducted in R using the aov functions.

Luminescence imaging and analysis

The luciferase activity in roots was visualized by time-lapse imaging of seedlings sprayed with 2 mM luciferin (Biosynth AG, Switzerland). DR5::Luciferase seedlings were grown using the general procedure as described above. To perform time-lapse imaging of the DR5:Luciferase expression in the oscillation zone, a Vers Array XP camera system (Roper Scientific) was used to image the luciferase signal in the vertical growing Arabidopsis root tip from 5 days old (4 to 8 seedlings) with the set-up of the exposure times of 5 min (binning 2) interrupted by 14 min LED WL (measured irradiances of 10~30 μmol m^-2 s^-1 for low light, 40~60 μmol m^-2 s^-1 for medium light and 110~130 μmol m^-2 s^-1 for high light condition) followed by 1 min darkness. The temperature in the imaging chamber was configured at either 21°C or 29°C by a recirculating Cooler (JULABO FL300). Image sequences were saved for further analysis in Fiji/ImageJ. Image sequences were converted into kymographs by tracking the final course of root growth. This visualization captures spatiotemporal changes in Luciferase signals during primary root growth. To quantify the universal DR5 signal in primary roots, the grey value of the primary root excluding the tip to the oscillation zone was recorded from the kymograph at an interval of every 10 hours. The PBS were counted manually from the kymographs and original image sequences. The length of primary roots was measured manually from the original images. To determine the time and strength of the systemic DR5 signal in primary roots, the time point and grey value were recorded when the systemic DR5 signal in the primary roots reached the top value. All measurements were performed with Fiji/ImageJ. The significance test was conducted in R using the t.test and aov functions. The Anderson-Darling normality test was conducted in R using the ad.test function.

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Two distinct oscillatory auxin signals define the plasticity of lateral rooting in Arabidopsis thaliana

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Abstract

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Introduction

Light quantitatively controls a systemic oscillatory auxin signal

Systemic auxin signal oscillations define PBS identity

Systemic auxin signal controls PBS identity at high ambient temperature

Light perception gates high temperature-dependent control of auxin-reliant PBS identity

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