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Functional redundancy in the control of seedling growth by the karrikin signaling pathway

Abstract

Main conclusion

SMAX1 and SMXL2 control seedling growth, demonstrating functional redundancy within a gene family that mediates karrikin and strigolactone responses.

Strigolactones (SLs) are plant hormones with butenolide moieties that control diverse aspects of plant growth, including shoot branching. Karrikins (KARs) are butenolide molecules found in smoke that enhance seed germination and seedling photomorphogenesis. In Arabidopsis thaliana, SLs and KARs signal through the α/β hydrolases D14 and KAI2, respectively. The F-box protein MAX2 is essential for both signaling pathways. SUPPRESSOR OF MAX2 1 (SMAX1) plays a prominent role in KAR-regulated growth downstream of MAX2, and SMAX1-LIKE genes SMXL6, SMXL7, and SMXL8 mediate SL responses. We previously found that smax1 loss-of-function mutants display constitutive KAR response phenotypes, including reduced seed dormancy and hypersensitive growth responses to light in seedlings. However, smax1 seedlings remain slightly responsive to KARs, suggesting that there is functional redundancy in karrikin signaling. SMXL2 is a strong candidate for this redundancy because it is the closest paralog of SMAX1, and because its expression is regulated by KAR signaling. Here, we present evidence that SMXL2 controls hypocotyl growth and expression of the KAR/SL transcriptional markers KUF1, IAA1, and DLK2 redundantly with SMAX1. Hypocotyl growth in the smax1 smxl2 double mutant is insensitive to KAR and SL, and etiolated smax1 smxl2 seedlings have reduced hypocotyl elongation. However, smxl2 has little or no effect on seed germination, leaf shape, or petiole orientation, which appear to be predominantly controlled by SMAX1. Neither SMAX1 nor SMXL2 affect axillary branching or inflorescence height, traits that are under SL control. These data support the model that karrikin and strigolactone responses are mediated by distinct subclades of the SMXL family, and further the case for parallel butenolide signaling pathways that evolved through ancient KAI2 and SMXL duplications.

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Abbreviations

KAR:

Karrikin

SL:

Strigolactone

KL:

KAI2 ligand

SMAX1 :

SUPPRESSOR OF MAX2 1

SMXL :

SMAX1-LIKE

D3 (14, 53) :

DWARF3 (14, 53)

PIN1 :

PIN-FORMED1

KAI2 :

KARRIKIN INSENSITIVE2

MAX2 :

MORE AXILLARY GROWTH2

DLK2 :

D14-LIKE2

KUF1 :

KAR-UP F-BOX1

IAA1 :

INDOLE-3-ACETIC ACID INDUCIBLE1

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Acknowledgments

Funding from the National Science Foundation (IOS-1350561) to D.C.N. and NIGMS National Institutes of Health Award T32GM007103 to N.M. supported this work.

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Correspondence to David C. Nelson.

Additional information

A contribution to the special issue on Strigolactones.

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Stanga, J.P., Morffy, N. & Nelson, D.C. Functional redundancy in the control of seedling growth by the karrikin signaling pathway. Planta 243, 1397–1406 (2016). https://doi.org/10.1007/s00425-015-2458-2

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  • DOI: https://doi.org/10.1007/s00425-015-2458-2

Keywords

  • Leaf morphology
  • MAX2
  • rac-GR24
  • Seed germination
  • Seedling photomorphogenesis
  • Strigolactone