Specialisation within the DWARF14 protein family confers distinct responses to karrikins and strigolactones in Arabidopsis

Abstract

SUMMARYKarrikins are butenolides derived from burnt vegetation that stimulate seed germination and enhance seedling responses to light. Strigolactones are endogenous butenolide hormones that regulate shoot and root architecture, and stimulate the branching of arbuscular mycorrhizal fungi. Thus, karrikins and strigolactones are structurally similar but physiologically distinct plant growth regulators. In Arabidopsis thaliana, responses to both classes of butenolides require the F-box protein MAX2, but it remains unclear how discrete responses to karrikins and strigolactones are achieved. In rice, the DWARF14 protein is required for strigolactone-dependent inhibition of shoot branching. Here, we show that the Arabidopsis DWARF14 orthologue, AtD14, is also necessary for normal strigolactone responses in seedlings and adult plants. However, the AtD14 paralogue KARRIKIN INSENSITIVE 2 (KAI2) is specifically required for responses to karrikins, and not to strigolactones. Phylogenetic analysis indicates that KAI2 is ancestral and that AtD14 functional specialisation has evolved subsequently. Atd14 and kai2 mutants exhibit distinct subsets of max2 phenotypes, and expression patterns of AtD14 and KAI2 are consistent with the capacity to respond to either strigolactones or karrikins at different stages of plant development. We propose that AtD14 and KAI2 define a class of proteins that permit the separate regulation of karrikin and strigolactone signalling by MAX2. Our results support the existence of an endogenous, butenolide-based signalling mechanism that is distinct from the strigolactone pathway, providing a molecular basis for the adaptive response of plants to smoke.

Strigolactones fine-tune the root system

“…1) (reviewed in Beveridge and Kyozuka 2010). In short, the first step of strigolactone biosynthesis involves the conversion of all-trans-β-carotene to 9-cis-β-carotene that is mediated by D27 (Waters et al 2012). Next, plastidic carotenoid cleavage dioxygenases 7 and 8 (CCD7 and CCD8 encoded, respectively, by MAX3 and MAX4 in Arabidopsis; Fig.…”

“…1) produce carlactone (Alder et al 2012). Carlactone (or another derived intermediate) is then transported to the cytosol where it is possibly converted to strigolactones by MAX1 that encodes a cytoplasmic cytochrome P450 enzyme (Booker et al 2005;Waters et al 2012). …”

Molecular mechanism of strigolactone perception by DWARF14

“…S1b). In addition, studies on a set of branching mutants of some plant species have indicated that the d14 and d3/max2/rms4 genes are closely related to a pathway downstream of SLs 1,2,13,14 ( Supplementary Fig. S1b).…”

“…D14 genes encode a/b-hydrolase family proteins [13][14][15][16] and their mutants exhibit a highly branched phenotype and are insensitive to SLs [13][14] . The d3/max2/rms4 mutants are also SL insensitive 1,2 .…”

“…The d3/max2/rms4 mutants are also SL insensitive 1,2 . D3/ MAX2/RMS4 genes encode members of the F-box-family protein [17][18][19][20] that participate in an Skp-cullin-F box (SCF) complex 18 and have diverse roles in the plant lifecycle 14,[21][22][23][24][25][26][27][28][29][30] . Recently, it has been reported that petunia DAD2, an orthologue of rice DWARF14 (D14) protein, can hydrolyse the enol ether linkage of GR24 and interacts with PhMAX2A, a petunia orthologue of Arabidopsis MAX2 protein, indicating that the formation of the DAD2-PhMAX2A complex initiates an SCF-mediated signal transduction pathway 31 .…”