Abstract
The butenolide molecule, karrikin (KAR), emerging in smoke of burned plant material, enhances light responses such as germination, inhibition of hypocotyl elongation, and anthocyanin accumulation in Arabidopsis. The KAR signaling pathway consists of KARRIKIN INSENSITIVE 2 (KAI2) and MORE AXILLARY GROWTH 2 (MAX2), which, upon activation, act in an SCF E3 ubiquitin ligase complex to target the downstream signaling components SUPPRESSOR OF MAX2 1 (SMAX1) and SMAX1-LIKE 2 (SMXL2) for degradation. How degradation of SMAX1 and SMXL2 is translated into growth responses remains unknown. Although light clearly influences the activity of KAR, the molecular connection between the two pathways is still poorly understood. Here, we demonstrate that the KAR signaling pathway promotes the activity of a transcriptional module consisting of ELONGATED HYPOCOTYL 5 (HY5), B-BOX DOMAIN PROTEIN 20 (BBX20), and BBX21. The bbx20 bbx21 mutant is largely insensitive to treatment with KAR2 , similar to a hy5 mutant, with regards to inhibition of hypocotyl elongation and anthocyanin accumulation. Detailed analysis of higher order mutants in combination with RNA-sequencing analysis revealed that anthocyanin accumulation downstream of SMAX1 and SMXL2 is fully dependent on the HY5-BBX module. However, the promotion of hypocotyl elongation by SMAX1 and SMXL2 is, in contrast to KAR2 treatment, only partially dependent on BBX20, BBX21, and HY5. Taken together, these results suggest that light- and KAR-dependent signaling intersect at the HY5-BBX transcriptional module.
Highlights
Karrikins (KARs) are a class of butenolide molecules found in the smoke of burned plant material that can induce germination of many plant species that emerge after fire (Dixon et al, 2009; Flematti et al, 2004; Nelson et al, 2012)
We find that B-BOX DOMAIN PROTEIN 20 (BBX20) and its close homolog BBX21 are essential for KARinduced inhibition of hypocotyl elongation and anthocyanin accumulation
RNA-sequencing (RNA-seq) analysis reveals largescale transcriptional changes in the smax1 smxl2 mutant, and we show that BBX20 and BBX21 are required for a subset of SUPPRESSOR OF MAX2 1 (SMAX1)/SMAX1-LIKE 2 (SMXL2)-dependent transcriptional regulation
Summary
Karrikins (KARs) are a class of butenolide molecules found in the smoke of burned plant material that can induce germination of many plant species that emerge after fire (Dixon et al, 2009; Flematti et al, 2004; Nelson et al, 2012). Germination of dormant Arabidopsis thaliana seeds can be stimulated by KARs (Nelson et al, 2009). KAR treatment enhances responses of seedlings to light. These responses include inhibition of hypocotyl elongation, enhancement of cotyledon expansion, and transcriptional upregulation of lightresponsive genes in Arabidopsis, and in Brassica tournefortii (Nelson et al, 2010; Sun et al, 2020). Six KARs have been detected in smoke extracts (KAR1 to KAR6) (Flematti et al, 2009; Hrdlicka et al, 2019), with KAR2 being most potent in Arabidopsis, inducing responses at the nanomolar to micromolar range (Nelson et al, 2010; Nelson et al, 2009)
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