A petunia ABC protein controls strigolactone-dependent symbiotic signalling and branching

Abstract

Strigolactones were originally identified as stimulators of the germination of root-parasitic weeds 1 that pose a serious threat to resource-limited agriculture 2 . They are mostly exuded from roots and function as signalling compounds in the initiation of arbuscular mycorrhizae 3 , which are plant-fungus symbionts with a global effect on carbon and phosphate cycling 4 . Recently, strigolactones were established to be phytohormones that regulate plant shoot architecture by inhibiting the outgrowth of axillary buds 5,6 . Despite their importance, it is not known how strigolactones are transported. ATP-binding cassette (ABC) transporters, however, are known to have functions in phytohormone translocation [7][8][9] . Here we show that the Petunia hybrida ABC transporter PDR1 has a key role in regulating the development of arbuscular mycorrhizae and axillary branches, by functioning as a cellular strigolactone exporter. P. hybrida pdr1 mutants are defective in strigolactone exudation from their roots, resulting in reduced symbiotic interactions. Above ground, pdr1 mutants have an enhanced branching phenotype, which is indicative of impaired strigolactone allocation. Overexpression of Petunia axillaris PDR1 in Arabidopsis thaliana results in increased tolerance to high concentrations of a synthetic strigolactone, consistent with increased export of strigolactones from the roots. PDR1 is the first known component in strigolactone transport, providing new opportunities for investigating and manipulating strigolactone-dependent processes.Strigolactones are a new class of carotenoid-derived 10 phytohormone in land plants. In addition to their role in shoot branching, strigolactones are exuded into the rhizosphere under phosphorus-limiting conditions 5 and act as growth stimulants of arbuscular mycorrhizal fungi 3 . To identify efflux carriers of arbuscular-mycorrhiza-promoting factors such as strigolactones, we used a degenerate primer approach ( Supplementary Fig. 2a) to isolate full-size PDR-type transporters (also known as ABC subtype G (ABCG) transporters) of P. hybrida that are abundant in phosphate-starved or mycorrhizal roots. The rationale behind the focus on these transporters, of which there are 15 in Arabidopsis 11 , 23 in Oryza sativa (rice) 11 and 23 putative factors in Solanum lycopersicum (tomato) ( Supplementary Fig. 3a), was that they are plasma membrane proteins often found in roots 12 , they are implicated in below-ground plantmicrobe interactions 13,14 , and they have affinities for compounds that are structurally related to strigolactones 8,9,15 . Of six primary candidates, only P. hybrida PDR1 had increased expression in roots that were subjected to either phosphate starvation (Fig. 1a) or colonization by the arbuscular mycorrhizal fungus Glomus intraradices (Fig. 1b). Furthermore, PDR1 transcript levels increased in response to treatment with the synthetic strigolactone analogue GR24 or the auxin analogue 1-naphthaleneacetic acid (NAA) (Fig. 1c). Auxin has been shown to upregulate strigolactone-bi...

Strigolactones fine-tune the root system

“…2) (Arite et al 2012;Guan et al 2012;Kretzschmar et al 2012). In support of the strigolactone-promoting primary root growth, Ruyter-Spira et al (2011) demonstrated that when grown without sucrose, GR24 applications trigger root growth in a MAX2-dependent manner.…”

“…More recently in petunia, an ATPbinding cassette (ABC) transporter PDR1 has been found to play a key role. pdr1 mutants display reduced symbiotic interactions because they are defective in strigolactone exudation, and have an enhanced branching phenotype, like other strigolactone mutants (Kretzschmar et al 2012). It will be interesting to discover whether and how this transporter exactly acts to control root to shoot distribution of strigolactones.…”

Phosphate Treatment Strongly Inhibits New Arbuscule Development But Not the Maintenance of Arbuscule in Mycorrhizal Rice Roots

“…Transcriptome analyses of mycorrhizal petunia roots under varying P conditions demonstrated the absence of defense responses and significant down-regulation of genes encoding enzymes of carotenoid and strigolactone biosynthesis (Breuillin et al, 2010). Biosynthesis, transport, and signaling events of strigolactone-related molecules are required for normal colonization (Floss et al, 2008;Vogel et al, 2010;Kretzschmar et al, 2012;Yoshida et al, 2012;Foo et al, 2013;Gutjahr et al, 2015). Strigolactones also induce hyphal branching (Akiyama et al, 2005) and increase the production of symbiotic fungal signals (Genre et al, 2013).…”

Diverse Roles of Strigolactone Signaling in Maize Architecture and the Uncoupling of a Branching-Specific Subnetwork

“…Rice D27 encodes a carotenoid isomerase (Lin et al, 2009;Alder et al, 2012;Waters et al, 2012a). In addition, an ATP-binding cassette transporter (Pleiotropic Drug Resistance1 [PDR1]) is implicated in SL transport (Kretzschmar et al, 2012). Recent biochemical analyses have resolved the early steps in the biosynthetic pathway in plastids.…”