The plant growth-promoting effect of an Ascophyllum nodosum (L.) extract derives from the interaction of its components and involves salicylic-, auxin- and cytokinin-signaling pathways

Abstract

Background

Ascophyllum Nodosum (L.) Extracts (ANE), even at low concentrations, are reported to behave as plant growth promoters and inducers of resistance to diverse abiotic and biotic stresses. However, the mechanisms regulating ANE's actions on plant metabolism have not been fully described. This study has two main objectives: (1) to investigate the role of some of the main components of an ANE extract on the plant growth-promoting action of ANE in Arabidopsis thaliana. To this end, experiments have been carried out studying the effect on plant growth of some of the main components of ANE at the concentration contained in the application rate of ANE extract. This study will allow us to obtain some insights about whether the ANE´s action may be ascribed to one or several of its components or derives from the ANE`s action as a whole and (2) to investigate the role of the signaling pathways regulated by salicylic acid (SA), indolacetic acid (IAA), and cytokinins (CK) in the mechanism of action behind the plant growth-promoting action of ANE. To this end, three Arabidopsis thaliana lines affected by the action of SA were treated with ANE: two loss-of-function mutants, pad4 (Phytoalexin Deficient 4) and sid2-2 (Salicylic acid Induction Deficient), along with a transgenic line expressing a bacterial salicylate hydroxylase, nahg, that prevents SA accumulation. ANE was also tested in an IAA loss-of-function mutant (tir1) and two CK receptors loss-of-function mutants (ahk2 and ahk3). Thus, the research advanced in the ANE´s mediated shoot growth-promoting mechanism of action through the coordinated signaling network involving SA-, CK-, and IAA-signaling pathways.

Results

The results revealed that: (1) the plant growth-promoting action of ANE seems to be related to the interaction of its components rather than to the action of some of its components and (2) the nahg transgenic line and the sid2-2 mutation, blocked the capacity of ANE to stimulate shoot growth. However, the pad4 mutant was stimulated by ANE. The fact that the action of ANE is impaired in sid2-2 and nahg indicates that the shoot growth-promoting effect of ANE is dependent on the SA-regulated signaling pathway. Likewise, the application of ANE to tir1, ahk2, and ahk3 plant mutants also affected the ANE´s capacity to promote shoot growth.

Conclusions

These results indicate that the ANE`s ability to stimulate shoot growth involves the coordinated activation of salicylic acid-, cytokinin-, and auxin-signaling pathways. The results obtained in the pad4 mutant indicate that the ANE´s action through the SA-signaling pathways that promote shoot growth differs from those regulated by the Enhanced Disease Susceptibility1/Phytoalexin Deficient4 (EDS1/PAD4) system. Finally, the action of ANE1 promoting plant growth seems to derive from the action of the extract as a whole.

Graphical Abstract