Abstract
The role of auxin in ripening strawberry (Fragaria ×ananassa) fruits has been restricted to the early stages of development where the growth of the receptacle is dependent on the delivery of auxin from the achenes. At later stages, during enlargement of the receptacle, other hormones have been demonstrated to participate to different degrees, from the general involvement of gibberellins and abscisic acid to the more specific of ethylene. Here we report the involvement of auxin at the late stages of receptacle ripening. The auxin content of the receptacle remains constant during ripening. Analysis of the transcriptome of ripening strawberry fruit revealed the changing expression pattern of the genes of auxin synthesis, perception, signaling and transport along with achene and receptacle development from the green to red stage. Specific members of the corresponding gene families show active transcription in the ripe receptacle. For the synthesis of auxin, two genes encoding tryptophan aminotransferases, FaTAA1 and FaTAR2, were expressed in the red receptacle, with FaTAR2 expression peaking at this stage. Transient silencing of this gene in ripening receptacle was accompanied by a diminished responsiveness to auxin. The auxin activity in the ripening receptacle is supported by the DR5-directed expression of a GUS reporter gene in the ripening receptacle of DR5-GUS transgenic strawberry plants. Clustering by co-expression of members of the FaAux/IAA and FaARF families identified five members whose transcriptional activity was increased with the onset of receptacle ripening. Among these, FaAux/IAA11 and FaARF6a appeared, by their expression level and fold-change, as the most likely candidates for their involvement in the auxin activity in the ripening receptacle. The association of the corresponding ARF6 gene in Arabidopsis to cell elongation constitutes a suggestive hypothesis for FaARF6a involvement in the same cellular process in the growing and ripening receptacle.
Highlights
Fruit ripening is a complex and coordinated irreversible developmental process that leads to the production of a soft and edible ripe fruit
The study of these components in different organ/cell scenarios has been useful to reveal their involvement in cellular processes such as cell division, cell enlargement (Velasquez et al, 2016), cell differentiation (Yang and Wang, 2016), and subcellular processes such as remodeling of the cell wall (Pacheco-Villalobos et al, 2016) and lignin biosynthesis (Zhang et al, 2014)
Our expression analysis of the genes encoding tryptophan amino transferases, whose in vitro activity of the enzymes has been demonstrated, supports that active auxin biosynthesis occurs in the green achenes and decreases thereafter
Summary
Fruit ripening is a complex and coordinated irreversible developmental process that leads to the production of a soft and edible ripe fruit. At early stage is believed to participate in the cell expansion associated to fruit growth, while at maturation a role has been proposed (Trainotti et al, 2007; McAtee et al, 2013), not definitive information exits on the cellular and molecular processes involved. Strawberry has been considered as an model to study the role played by the hormone auxin, at the molecular level, in fruit growth and ripening. It was reported that growth of the receptacle ceased if achenes, the source of auxin, were removed after pollination, but growth of the receptacle was taken up again after the external application of 2-naphtoxyacetic acid (Nitsch, 1950). The removal of the achenes accelerated some processes associated with fruit ripening (Given et al, 1988). Detailed studies on the content, synthesis, and signaling of this hormone in different fruit parts at different developmental stages are lacking
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