KAI2 regulates seedling development by mediating light-induced remodelling of auxin transport

Abstract

The photomorphogenic remodelling of seedling growth upon exposure to light is a key developmental transition in the plant life cycle. The α/β-hydrolase signalling protein KARRIKIN-INSENSITIVE2 (KAI2), a close homologue of the strigolactone receptor DWARF14 (D14), is involved in this process, and kai2 mutants have strongly altered seedling growth as a result. KAI2 and D14 both act through the MAX2 (MORE AXILLARY BRANCHING2) F-box protein to target proteins of the SMAX1-LIKE (SUPPRESSOR OF MAX2 1) (SMXL) family for degradation, but the signalling events downstream of this step are unclear in both pathways. Here, we show that kai2 phenotypes arise because of a failure to downregulate auxin transport from the seedling shoot apex towards the root system, rather than a failure to respond to light per se. We demonstrate that KAI2 controls the light-induced remodelling of the PIN-mediated auxin transport system in seedlings, promoting the reduction of PIN3, PIN4, and PIN7 abundance in older tissues, and the increase of PIN1, PIN2, PIN3, and PIN7 abundance in the root meristem, consistent with transition from elongation-mediated growth in the dark to meristematically-mediated growth in the light. We show that removing PIN3, PIN4 and PIN7 from kai2 mutants, or pharmacological inhibition of auxin transport and synthesis, is sufficient to suppress most kai2 seedling phenotypes. KAI2 is not required for the light-mediated changes in PIN gene expression but is required for the changes in PIN protein abundance at the plasma membrane; we thus propose that KAI2 acts to promote vesicle trafficking, consistent with previous suggestions about D14-mediated signalling in the shoot.

KAI2 promotes Arabidopsis root hair elongation at low external phosphate by controlling local accumulation of AUX1 and PIN2

“…DR5v2 pro :GFP expression was decreased in kai2 meristems with respect to the wild type, possibly due to reduced rootward flow of auxin through kai2 roots. 27 Importantly, and consistent with the RHL response, DR5v2 pro -driven GFP signal in kai2-2 increases to the level of the untreated wild type after treatment with NAA but does not change with 2,4-D (Figure 3E). Together, these results suggest there may be reduced influx carrier activity in kai2.…”

Karrikin signaling regulates hypocotyl shade avoidance response by modulating auxin homeostasis in Arabidopsis

“…These results, coupled with the recently reported research findings from Hamon‐Josse et al . (2021), increase the adaptive mechanisms by which KL signaling integrates the auxin hormone pathway to achieve adaptation to different light conditions.…”

“…Therefore, auxin seems to be one of the most important regulatory factors involved in the elongation of the hypocotyl during shade avoidance. A recent study showed that KAI2 controls the light‐induced remodeling of the PIN‐mediated auxin transport system in seedlings (Hamon‐Josse et al ., 2021). In summary, shade stress may regulate hypocotyl elongation by promoting auxin biosynthesis and/or transport.…”

“…Here, we speculate that the increase in the abundance of PIN7 leads to an increase in auxin transport into the surrounding tissue. The auxin leakage model has been hypothesized previously (Hamon‐Josse et al ., 2021; Villaécija‐Aguilar et al ., 2022). We proposed that this auxin leakage to external tissue may explain the increase in the growth of the main roots and lateral roots of kai2 and max2 mutants, which is an auxin‐driven process.…”

KARRIKIN UP-REGULATED F-BOX 1 (KUF1) imposes negative feedback regulation of karrikin and KAI2 ligand metabolism in Arabidopsis thaliana

“…KAI2 remodels auxin distribution in seedlings during photomorphogenesis, putatively by controlling the abundance of the auxin efflux carriers PIN1, PIN3, and PIN7 at the plasma membrane. This in turn influences hypocotyl elongation and root development ( 67 ).…”