The Physcomitrium (Physcomitrella) patens PpKAI2L receptors for strigolactones and related compounds function via MAX2-dependent and -independent pathways

Abstract

In angiosperms, the α/β hydrolase DWARF14 (D14), along with the F-box protein MORE AXILLARY GROWTH2 (MAX2), perceives strigolactones (SL) to regulate developmental processes. The key SL biosynthetic enzyme CAROTENOID CLEAVAGE DIOXYGENASE8 (CCD8) is present in the moss Physcomitrium patens, and PpCCD8-derived compounds regulate moss extension. The PpMAX2 homolog is not involved in the SL response, but 13 PpKAI2LIKE (PpKAI2L) genes homologous to the D14 ancestral paralog KARRIKIN INSENSITIVE2 (KAI2) encode candidate SL receptors. In Arabidopsis thaliana, AtKAI2 perceives karrikins and the elusive endogenous KAI2-Ligand (KL). Here, germination assays of the parasitic plant Phelipanche ramosa suggested that PpCCD8-derived compounds are likely non-canonical SLs. (+)-GR24 SL analog is a good mimic for PpCCD8-derived compounds in P. patens, while the effects of its enantiomer (−)-GR24, a KL mimic in angiosperms, are minimal. Interaction and binding assays of seven PpKAI2L proteins pointed to the stereoselectivity towards (−)-GR24 for a single clade of PpKAI2L (eu-KAI2). Enzyme assays highlighted the peculiar behavior of PpKAI2L-H. Phenotypic characterization of Ppkai2l mutants showed that eu-KAI2 genes are not involved in the perception of PpCCD8-derived compounds but act in a PpMAX2-dependent pathway. By contrast, mutations in PpKAI2L-G, and -J genes abolished the response to the (+)-GR24 enantiomer, suggesting that PpKAI2L-G, and -J proteins are receptors for moss SLs.

Masks Start to Drop: Suppressor of MAX2 1-Like Proteins Reveal Their Many Faces

“…Finally, members of one of the SMXL clades in moss, dubbed SMXLC, lack the D1 domain ( Walker et al, 2019 ), which might potentially correlate with a loss or change of their ability to interact with an α/β-hydrolase. Although KAI2-like receptors independently acquired SL sensitivity in P. patens , this SL perception and signaling occurs independently of PpMAX2 ( Lopez-Obando et al, 2018 , 2021 ). Although SMXLs would need their D1 domain in canonical SL signaling, the independently evolved SL signaling pathway in moss might also differ in this regard.…”

“…Despite the presence of the SL biosynthesis enzymes D27, CAROTENOID CLEAVAGE DIOXYGENASE (CCD) 7, CCD8, and MAX1 in most nonseed plants, the canonical SL receptor D14 is only found in seed plants ( Bythell-Douglas et al, 2017 ; Walker et al, 2019 ), leading to the assumption that SLs first acted as symbiotic signals in the rhizosphere, rather than as plant development-regulating phytohormones ( Kodama et al, 2021 ). Interestingly, most nonvascular land plants possess additional KAI2-like receptors, whereas in the moss P. patens , they appear to have evolved independently from D14 to act as SL receptors ( Bythell-Douglas et al, 2017 ; Lopez-Obando et al, 2021 ). This SL sensitivity emergence in mosses is correlated with the acquisition of a second clade of SMXLs ( Walker et al, 2019 ), allowing us to speculate that these additional SMXLs have been recruited as SL signaling targets ( Figure 2A ).…”

“…Independently, a similar event has seemingly occurred at the origin of the angiosperms, when the SMAX1 lineage split into aSMAX1 and aSMXL7/8 ( Walker et al, 2019 ). However, SL signaling in P. patens does not depend on MAX2, suggesting that this comparison is not entirely reliable and that functional examination of SMXL homologs in mosses is still needed to uncover their precise role ( Lopez-Obando et al, 2021 ).…”

“…In contrast to D14, KAI2 is found in all sequenced land plant genomes and in some charophyte algae, suggesting that KAI2-MAX2-dependent signaling is ancestral and that D14 probably evolved through duplication and neofunctionalization of KAI2 ( Delaux et al, 2012 ; Bythell-Douglas et al, 2017 ). Interestingly, the ability to perceive SLs has been proposed to have arisen at least additionally twice in the evolution of land plants, because both the moss Physcomitrium patens and the parasitic plant species from the Orobanchaceae family possess KAI2-like SL-sensitive receptors ( Conn et al, 2015 ; Xu et al, 2018 ; Lopez-Obando et al, 2021 ).…”

Expansion of the Strigolactone Profluorescent Probes Repertory: The Right Probe for the Right Application

“…In seed plants, SL perception as phytohormone involves a receptor called, DWARF14 (D14), [OsD14 in rice, AtD14 in Arabidopsis, RAMOSUS3 (RMS3) in pea, DECREASED APICAL DOMINANCE2 (DAD2) in petunia] which belongs to the α/β hydrolase family with a conserved catalytic triad (Ser, His, Asp; Arite et al, 2009 ; Hamiaux et al, 2012 ; Waters et al, 2012 ; de Saint Germain et al, 2016 ; Yao et al, 2016 ). In Physcomitrium patens and in obligate root parasitic plants, SLs are perceived by their ancestral paralogs, HYPOSENSITIVE TO LIGHT/KARRIKIN INSENSITIVE2 (HTL/KAI2) (Conn et al, 2015 ; Toh et al, 2015 ; de Saint Germain et al, 2021b ; Lopez-Obando et al, 2021 ; Mizuno et al, 2021 ), referred hereinafter as KAI2s.…”