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Shoot and root thermomorphogenesis are linked by a developmental trade-off

Christophe Gaillochet, Yogev Burko, Matthieu Pierre Platre, Ling Zhang, Jan Simura, Vinod Kumar, Karin Ljung, Joanne Chory, Wolfgang Busch

Preprint posted on May 13, 2020 https://www.biorxiv.org/content/10.1101/2020.05.07.083246v2.full

Let there be light...or temperature? Light signalling players HY5, COP1 and PHYA,B are required for root thermomorphogenesis.

Selected by Alvaro Montiel-Jorda

Background

Plants are sessile organisms, anchored to the soil. In contrast to their animal counterparts, they cannot escape from unfavorable changes in environmental conditions such as heat or drought; nor can they distance themselves from the attack of pathogens. They must therefore be able to integrate a plethora of stimuli to successfully complete their life cycle and give rise to new progeny. This ability is known as “plasticity”, meaning that plants can effectively modulate their developmental programs in response to external cues in order to increase their fitness in the new setting. A clear example would be plants growing in a canopy. In such environment, taller plants have more access to sunlight, in turn neglecting smaller ones to access it. As a result, smaller plants respond by increasing their growth as to be able to obtain sunlight.

Thermomorphogenesis is defined as the influence of high ambient temperature on plant development (Quint et al. 2016). It should be noted that thermomorphogenesis and heat stress or shock are not the same thing. During thermomorphogenesis, plants grow under a higher temperature than usual yet not harmful to them, as corroborated by the absence of expression of heat stress markers (Kumar and Wigge 2010). Thermomorphogenesis has mostly been studied in aerial tissues and processes (hypocotyl, petioles, leaves, flowering), whereas roots have been almost completely neglected. Thermomorphogenesis-associated phenotypes include: hypocotyl and petiole elongation, leaf hyponasty and early flowering (Fig.1).

Molecular and genetic control of plant thermomorphogenesis ...

Figure 1. Thermomorphogenesis-related phenotypes. Adopted from Quint et al., 2016. 

These phenotypes rely on the transcription factor PHYTOCHROME-INTERACTING 4 (PIF4), often referred to as “the master regulator of thermomorphogenesis”, since they are all abolished in the pif4 mutant (Koini et al., 2008).  It has been shown that upon elevated ambient temperature, PIF4 triggers a local auxin accumulation that produces these developmental changes in the aerial plants of the plant.

However, things are less clear when it comes to roots, where a debate sparked as to whether auxin and PIF4 are or not required for root thermomorphogenesis. Here, Gaillochet et al., settle the debate using genetics and high-throughput phenotyping. Their data strongly supports a role for auxin in root thermomorphogenesis but not for PIF4 and opens up many new questions.

Key findings

In this study, the authors use the power of genetics to unequivocally uncover the main players in plant root thermomormphogenesis. Since many genes involved in light signaling are also important for aerial thermomorphogenesis, the authors decided to test if that was the case for HY5, COP1 and PHYA/B.

Indeed, the hy5cop1, and phyA/B mutants were not able to elongate the root in response to increased temperature to the same extent as wild-type. This suggests that an until now believed to be a shoot-specific regulatory module could also play a role in roots. It will now be highly interesting to test whether SPAs, CRYs and other proteins involved in light signaling are also required for root thermomorphogenesis. Interestingly, HY5 is a mobile transcription factor that can travel from shoots to roots (Chen et al., 2016).  Therefore, the authors sought to determine whether local HY5 only expressed in shoots would be able to complement the mutant and thus allow temperature-induced root elongation. To do that, they expressed HY5 under the control of the CAB3 promoter, which resulted in shoot-specific HY5 expression, compared to the CER6 promoter, which resulted in detectable HY5 in both tissues. Surprisingly, shoot-localized local HY5 is enough to rescue the mutant (Fig.2).

 

Figure 2. Shoot-specific complementation of the hy5 mutant is enough to achieve complementation.

The other focus of the paper is to end the debate on the importance of auxin and PIFs in root thermomorphogenesis. For the past couple of years, there has been a debate as to whether auxin signaling is required or not for root thermomorphogenesis. Early work from the groups led by Mark Estelle and Abidur Rahman seemed to point at auxin as indeed being crucial for root thermomorphogenesis (Hanzawa et al., 2013; Wang et al., 2016). However, this theory was rapidly challenged by the group of Grégory Vert, who suggested instead that auxin signaling is actually dispensable and it is rather brassinosteroid signaling who controls this response (Martins and Montiel-Jorda, 2017).

Here, Gaillochet et al., use higher the order mutant yucQ (mutant for YUCCAs 3/5/7/8/9) to assess the role of auxin biosynthesis and find out, contrary to the simple yuc8 mutant, that it has a phenotype (Fig.3). This result is somewhat shocking taking into account that despite TAA1 being upstream of YUCCAs (Mashiguchi et al., 2011), the taa1 behaves as the wild type when it comes to root thermomorphogenesis (Martins and Montiel-Jorda, 2017). However, auxin biosynthesis is still far from being completely understood, and this result could imply that the auxin biosynthetic route differs between shoots and roots, or between 21 and 26ºC.

Similarly, the authors claim that the tir1afb2 mutant is impaired in root thermomorphogenesis, contrary to what was reported by Martins and Montiel-Jorda, 2017. This result could be due to differences in the experimental setup, including growing conditions. They also find out that non-canonical auxin signaling (going through plasma membrane-localized TMKs) is also necessary for root thermomorphogenesis (Fig.3), which begs the question, which one, canonical or non-canonical is more important for thermomorphogenesis? Do they contribute equally?

Figure 3. Phenotyping of several auxin mutants proves both canonical and non-canonical auxin signaling are required for root thermomorphogenesis.

The finding that PIF4 and PIF5 are not required for root thermomorphogenesis was shocking (Martins and Montiel-Jorda, 2017) and therefore contested. Here, the authors test if that is always the case under their own growth conditions and find exactly the same phenotype. Moreover, they also confirm that neither PIF1 nor PIF3 play a role in root thermomorphogenesis since the pifQ (mutant for PIFs 1/3/4/5/) responds to temperature as WT. It seems that PIF7 is also important for shoot thermomorphogenesis (Chung et al., 2020; Fiorucci et al., 2020), so root thermomorphogenesis might still require a PIF!

What I like about this work

I chose this paper because of several reasons. Firstly, it uncovers new factors involved in root thermomorphogenesis unknown until now. Secondly, it points at the importance of the gene expression pattern when looking at a mutant phenotype. I believe many groups will soon try to complement several root thermomorphogenesis mutants with shoot and root-specific expression. Thirdly, this paper answers complicated questions such as the role of auxin in root thermomorphogenesis yet opening new ones at the same time.

Acknowledgements

I would like to thank the authors for answering the questions and engaging in the discussion!

Further reading

Quint, M., Delker, C., Franklin, K. A., Wigge, P. A., Halliday, K. J., & van Zanten, M. (2016). Molecular and genetic control of plant thermomorphogenesis. Nature plants2(1), 1-9.

Koini, M. A., Alvey, L., Allen, T., Tilley, C. A., Harberd, N. P., Whitelam, G. C., & Franklin, K. A. (2009). High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Current Biology19(5), 408-413.

Martins, S., Montiel-Jorda, A., Cayrel, A., Huguet, S., Paysant-Le Roux, C., Ljung, K., & Vert, G. (2017). Brassinosteroid signaling-dependent root responses to prolonged elevated ambient temperature. Nature communications8(1), 1-11.

Hanzawa, T., Shibasaki, K., Numata, T., Kawamura, Y., Gaude, T., & Rahman, A. (2013). Cellular auxin homeostasis under high temperature is regulated through a SORTING NEXIN1–dependent endosomal trafficking pathway. The Plant Cell25(9), 3424-3433.

Wang, R., Zhang, Y., Kieffer, M., Yu, H., Kepinski, S., & Estelle, M. (2016). HSP90 regulates temperature-dependent seedling growth in Arabidopsis by stabilizing the auxin co-receptor F-box protein TIR1. Nature communications7(1), 1-11.

Kumar, S. V., & Wigge, P. A. (2010). H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell140(1), 136-147.

Chen, X., Yao, Q., Gao, X., Jiang, C., Harberd, N. P., & Fu, X. (2016). Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Current Biology26(5), 640-646.

Mashiguchi, K., Tanaka, K., Sakai, T., Sugawara, S., Kawaide, H., Natsume, M., … & McSteen, P. (2011). The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences108(45), 18512-18517.

Tags: arabidopsis, light, roots, thermomorphogenesis

Posted on: 3rd July 2020 , updated on: 6th July 2020

doi: https://doi.org/10.1242/prelights.20816

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Author's response

Christophe Gaillochet shared

1) Your data proves that PIF1,3,4 and 5 are not required for root thermomorphogenesis. However, there are others PIFs that could mimic the role of PIF4 in shoots. It has recently been discovered (Chung et al., 2020; Fiorucci et al., 2020) that PIF7 is important for temperature-induced hypocotyl elongation. Have you tested if that is the case?

We are currently testing how pif7 and pif1,3,4,5,7 root respond to increased ambient temperature. We should soon provide data to answer this point.

2) TAA1 is believed to be upstream of YUCCAs in the auxin biosynthetic pathway (Mashiguchi et al., 2011). Yet, the taa1 mutant is not affected in root thermomorphogenesis (Martins and Montiel-Jorda, 2017) but your yuccaQ is. Can you propose an explanation for this result?

I think that the fact that we observe reduced growth response in yucQ -whereas interfering with one upstream regulator such as taa1 does not- could be explained by functional redundancy at the level of TAA1. It was shown that TAR1 and TAR2 can carry overlapping function with TAA1 (Stepanova 2008) and thus I think that YUC activity in taa1 as well as auxin levels are sufficient to allow roots to elongate as wild type.

3) Both auxin signaling pathways, canonical and TMK-based seem to be required for root thermomorphogenesis. Do you think that they contribute equally to root thermomorphogenesis or that one could be more important than the other?

That’s a great question! Based on recent reports from Tongda Xu lab (Cao, 2019; Wang 2020) who has analyzed this process in different developmental contexts, I think that auxin signals might be integrated through both pathways. However, it is not clear to me whether one might be more important during root thermomorphogenesis. It would be interesting to further investigate how the TMKs and TIR/AFB system interact at the molecular and temporal level during thermomorphogenesis.

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