Context

Strigolactones (SLs) are one of the most recently discovered hormone signalling pathways in plants and their nature and evolution are still enigmatic. SLs are a complex group of carotenoid-derived terpenoid lactones unique to plants. As phytohormones, they control various aspects of plant growth, including shoot branching, root growth and senescence, in addition to their function as rhizosphere-signalling molecules for arbuscular mycorrhizal symbiosis.

In seed plants, SLs are perceived by the protein DWARF14 (D14). Structurally similar to SLs, karrikins are perceived by the paralog receptors KARRIKIN INSENSITIVE2 (KAI2). Karrikins are by products of burning plants and work as a signal to detect smoke in the environment. It is proposed that there is an endogenous compound similar to karrikins referred to as KAI2-ligand (KL) that acts as a hormone but its chemical nature is still elusive. The KL signalling pathway seems to be even more ancestral than SL perception and biosynthesis. Thus, KL and SL are two branches of two hormonal signalling pathways that evolved together and share several components. These pathways also involve MAX2 F-box proteins that interact with KAI2 and subsequently trigger the degradation of SMXL transcription factor-like proteins.

Most components of SL/KL biosynthesis, perception and signal transduction were characterized in flowering plants but are conserved across land plants (Walker et al., 2019). In the last few years, biochemical studies have characterized proteins of SL/KL pathway from non-flowering plants, particularly in the models bryophytes Marchantia polymorpha and Physcomitrium patens (Bürger et al., 2019; Waters et al., 2015). Both models lack some of the SL biosynthesis components identified in flowering plants. Especially, MAX1 is not present in both and a CCD8 ortholog is lacking in M. polymorpha. It is likely that other proteins could replace these components, challenging the notions of what is “canonical” in the pathway. In some cases, these proteins could have been replaced by homologous proteins as in the case of D14 and KAI2. Biochemical studies have provided important hints on how this signalling pathway may work in bryophytes but functional studies using mutant plants are lacking.

Figure 1. Schematic model for KL and SL signalling in P. patens growth in wild-type and mutant backgrounds and in response to two GR24 enantiomers (SL analogues). see Lopez-Obando et al. Figure 13 for full reference.

Major findings

In two recent pre-prints, Mizuno et al. and Lopez-Obando et al., provide novel insight about the KAI2-mediated signalling pathway in M. polymorpha and P. patens, respectively. In P. patens,  the importance of CCD8 SL-like biosynthesis activity in plant growth and development was previously demonstrated (Proust et al., 2011). Here, Lopez-Obando and colleagues take an original approach using Phelipanche ramosa, a parasitic plant that germinates in response to host plant SL/KL. This allows testing PpCCD8-derived compound activity using P. patens exudates from wild-type and Ppccd8 mutants. In one of the seed populations, only wild-type exudates presented germination stimulant activity. This greatly contributes to the idea that P. patens can synthesize active SLs in a CCD8 conserved pathway, despite lacking MAX1.

As shown before, neither M. polymorpha nor P. patens phenotypically respond to the karrikins generated by burning vegetation as in the KL pathway of flowering plants. However, both pre-prints showed that KAI2 enzymes can potentially interact with SL analogues, possibly connecting both branches of the “canonical” signalling pathway in the common ancestor of land plants and during evolution. Mizuno et al. managed to create a full mutant plant for KAI2 thanks to the M. polymorpha genome only bearing two copies of the gene. Remarkably, Marchantia Mpkai2 mutant plants displayed developmental defects similar to Mpmax2 mutants. In the other hand, in P. patens with 13 KAI2-like genes, it represented a more difficult task. Thus, Lopez-Obando et al. generated multiple mutants of combinations of P. patens KAI2 corresponding to different clades. Particularly one of these clades, mutant plants phenocopy not on Ppmax2 but also Ppccd8. These results suggest that KAI2 and the F-box MAX2 participate in the genetic pathway regulating growth and photomorphogenesis in a conserved fashion, but in P. patens, some KAI2 genes probably diversified into MAX2 independent pathways. In M. polymorpha, Mpkai2 and Mpmax2 showed a slightly reduced sensibility to synthetic SL analogues.

In addition to functional studies of KAI2 and MAX2, Mizuno et al. also analyzed MpSMXL genes. MpSMXL is also degraded through ubiquitination as in flowering plants. Interestingly, they found that Mpsmxl double mutants can suppress mutant phenotypes in Mpkai2 or Mpmax2 backgrounds. Moreover, the complementation of Mpsmxl with a version of MpSMXL resistant to protein degradation showed similar phenotypes to Mpkai2 and Mpmax2, suggesting that SMXL degradation could be a conserved part of the SL/KL pathway despite the strong divergence of this family (Walker et al., 2019).

Future directions

Current knowledge supports the hypothesis that there is a SL/KL signalling pathway conserved in the common ancestor to land plants that probably works in a similar way in extant bryophytes. Nevertheless, many aspects of the evolution of SL/KL biosynthesis and signalling pathways are poorly understood. It is clear that bryophyte components are unable to replace their putative counterparts in flowering plants as shown by Lopez-Obando et al. and also before (Bürger et al., 2019; Waters et al., 2015), indicating that the involved interactions may have co-evolved differently in each lineage. It remains to be tested whether SMXL proteins could also participate in the pathway in P. patens. In P. patens, it seems that SL compounds can be synthesized through CCD8 as in flowering plants, while in M. polymorpha, only the KL branch may be functional. In that sense, Lopez-Obando et al. propose in this pre-print that the diversification of KAI2 receptors could be important to separate both branches in P. patens. In this context, the role of MAX2 may be restricted to KL signalling (Lopez-Obando et al., 2016). The main challenge is still the lack of a canonical KL compound that could be unequivocally associated with KAI2 receptors. KAI2 diversity and promiscuity to synthetic SL analogues are often problematic and controversial in experimental conditions. Another exciting open question is how arbuscular mycorrhizal symbiosis is affected in the bryophyte mutants of KL/SL signalling and biosynthesis components.

What I Liked

These two new studies reach to complementary conclusions and provide many insights (some of them were not mentioned here) that will help to complete the puzzle of the SL/KL pathway in bryophytes. They also highlight the importance of the use of multiple model systems to address complex evolutionary challenges. An evolutionary framework will certainly facilitate the generation of new hypotheses leading to a better understanding of this complex and diversified signalling pathway.

References

Bürger, M., Mashiguchi, K., Lee, H.J., Nakano, M., Takemoto, K., Seto, Y., Yamaguchi, S., Chory J. (2019). Structural basis of karrikin and non-natural strigolactone perception in Physcomitrella patens. Cell Reports, 26(4):855-865.e5. https://doi.org/10.1016/j.celrep.2019.01.003.

Lopez‐Obando, M., de Villiers, R., Hoffmann, B., Ma, L., de Saint Germain, A., Kossmann, J., Coudert, Y., Harrison, C.J., Rameau, C., Hills, P. and Bonhomme, S. (2018), Physcomitrella patens MAX2 characterization suggests an ancient role for this F‐box protein in photomorphogenesis rather than strigolactone signalling. New Phytol, 219: 743-756. https://doi.org/10.1111/nph.15214

Waters, M.T., Scaffidi, A., Moulin, S.L.Y., Sun, Y.K., Flematti, G.R., Smith S.M. (2015). A Selaginella moellendorffii ortholog of KARRIKIN INSENSITIVE2 functions in Arabidopsis development but cannot mediate responses to karrikins or strigolactones. The Plant Cell Jul 2015, 27(7):1925-1944. https://doi.org/10.1105/tpc.15.00146

Proust, H., Hoffmann, B., Xie, X., Yoneyama, K., Schaefer, D.G., Yoneyama, K., Nogué, F., Rameau, C. (2011). Strigolactones regulate protonema branching and act as a quorum sensing-like signal in the moss Physcomitrella patens. Development 138:1531-1539. https://doi.org/10.1242/dev.058495

Walker, C.H., Siu-Ting, K., Taylor, A., et al (2019). Strigolactone synthesis is ancestral in land plants, but canonical strigolactone signalling is a flowering plant innovation. BMC Biol 17:70. https://doi.org/10.1186/s12915-019-0689-6

Tags: evodevo, marchantia, physcomitrella, strigolactones

doi: https://doi.org/10.1242/prelights.25988

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