Commentary

Emerging trends in strigolactoneresearch

In 2008, back-to-back publications in the journal Nature revealedthat strigolactones are a new class of plant hormones that controlshoot architecture by inhibiting axillary bud growth (Gomez-Roldan et al., 2008; Umehara et al., 2008). Since then, strigolac-tones have been established as an important group of plant growthregulators that affect a raft of different plant processes (see reviewBrewer et al., 2013). In this issue of New Phytologist, a surprisingnew role of strigolactones in stolon and tuber development isrevealed by Pasare et al. (pp. 1108–1120) that adds support toemerging theories of strigolactone involvement in resource parti-tioning.

‘Why then do the strigolactone-deficient CCD8-RNAi

plants have less, not more, stolons?’

Pasare et al. used RNAi technology to generate potato plantswith reduced expression of CCD8, a key gene in the strigolactonebiosynthesis pathway. The resultant plants had significantlyreduced strigolactone content and displayed many of the traitsobserved in other strigolactone-deficient plants, such as increasedaxillary shoot branching and decreased plant height. However, themost intriguing discovery is the effect of strigolactone deficiency onstolon (underground stem) development; the CCD8-RNAi plantshad reduced stolon formation, with typically fewer and smallertubers. Strigolactone deficiency also had a dramatic effect on thegrowth habit of the stolons such that the majority of the stolonsshowed a loss of diageotropic growth pattern, emerging above-ground instead of growing horizontally outwards into the soil.

These discoveries are important on a number of levels; first, thesefindings have large implications for improving the pre- and post-harvest traits of the potato, which will likely have many beneficialflow-on effects for the economically important potato industriesaround the world. Second, from a biology perspective, every newplant process that strigolactones are found to regulate brings us astep closer to understanding the mechanism(s) of strigolactonefunction. To date, we still know very little about how strigolactoneselicit their effects on plant development; however, evidence isstarting to emerge that indicates that strigolactones appear tofunction by modulating auxin transport, cell division/meristemdormancy, and resource partitioning. These are not mutuallyexclusive and, in fact, it is likely that each strigolactone-regulated

process involves a combination of two, or all three of thesemechanisms.

Strigolactones modulate auxin transport

Plants with defects in strigolactone synthesis have been found tohave higher rates of auxin movement through the polar auxintransport stream (Brewer et al., 2009; Shinohara et al., 2013). Thehigher auxin transport rate appears to be due to increased levels ofthe auxin transporter, PIN1 in the strigolactone mutants.Consistent with these findings, the synthetic strigolactone, GR24,causes a reduction in polar auxin transport in a dose dependentmanner. Recently, it was revealed that GR24 is able to reduceauxin transport by rapidly promoting endocytosis of PIN1(Shinohara et al., 2013). With less PIN1 on the plasma mem-brane, the rate at which auxin can be transported out of the celldecreases.

The effect of strigolactones on PIN1 has led some researchers tohypothesize that by inhibiting auxin transport out of buds,strigolactones are able to prevent axillary bud outgrowth (Shino-hara et al., 2013). However, a number of studies have now revealedthat the relationship between polar auxin transport and axillary budoutgrowth is more complicated than first thought (Ferguson &Beveridge, 2009). For example, disruption to auxin transport bystem girdling or chemical treatment does not always correlate withaxillary bud outgrowth, indicating that there are likely other, as yet,unknown mechanisms that are also important for apical domi-nance.Moreover, chemically reducing the rate of auxin transport inthe strigolactonemutants to wild-type levels results in only a partialrestoration of their branching phenotype (Bennett et al., 2006).These results indicate that modifying auxin transport is only one ofthe mechanisms employed by strigolactones to inhibit axillary budgrowth.

Strigolactones regulate cell division/meristemdormancy

The ability of strigolactones to limit adventitious rooting byinhibiting the initial formative divisions of the founder cells(Rasmussen et al., 2012) indicates that strigolactones may beable to regulate cell division in specific tissues within the plant.Consistent with this, strigolactones have been found to induce celldivision in interfascicular cambium tissues within plant stems(Agusti et al., 2011). Furthermore, in axillary buds, strigolactonespromote the expression of BRANCHED1 (BRC1), a key transcrip-tional regulator of bud dormancy that is thought to be involved inthe maintenance of the stem cell niche, cell division, and lateralorgan initiation (Dun et al., 2012). These results indicate that oneof the functions of strigolactones is to modulate cell division andmeristem dormancy in specific tissues.

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Interestingly, cytokinin inhibits the expression of BRC1 and acombination of strigolactone and cytokinin results in intermediateexpression (Dun et al., 2012). Bud outgrowth appears to bedetermined by the ratio of strigolactone to cytokinin in buds whichact, at least in part, through BRC1. BRC1 is not the only commontarget of these two hormones; cytokinin, like strigolactone, alsoregulates auxin transport by promoting PIN1 removal from theplasma membrane (Marhavy et al., 2011). These results indicatethat one of strigolactone’s mechanisms of action may be tomodulate cytokinin action through common targets. It remains tobe determinedwhether strigolactones can also target the same genesthrough which cytokinins regulate the cell cycle (Hwang et al.,2012).

Strigolactones modulates resource partitioning inplants

It is now becoming apparent that strigolactones play an importantrole in maintaining phosphate and nitrogen homeostasis in plants.Consistent with previous findings (Yoneyama et al., 2007), Pasareet al. report that strigolactone levels significantly increase underphosphate-limiting conditions. A likely reason for this rise instrigolactone in some plant species is to enhance the associationwith arbuscular mycorrhizal fungi in order to improve phosphateuptake from the rhizosphere. Additionally, the ability of strigolac-tones to modify plant growth (e.g. shoot branching, lateral rootinitiation, root hair production; Koltai, 2011) supports a role forstrigolactones in regulating the flow of plant resources towardsspecific tissues to provide the plant with the best chance of long-term survival in suboptimal conditions (Brewer et al., 2013).

Now, Pasare et al. present further evidence supporting a role forstrigolactones in regulating resource allocation. The finding thatthe CCD8-RNAi plants have decreased stolon formation isintriguing given that stolons are stem branches that originate fromaxillary buds towards the base of the main stem. Why then do thestrigolactone-deficient CCD8-RNAi plants have less, not more,stolons? In strigolactone-deficient pea plants, not all axillary budsgrow out and the pattern of bud outgrowth is influenced byenvironmental conditions (Beveridge et al., 2003). These resultsindicate the possibility that additional signals may act through, orin conjunction with strigolactones to regulate resource partitioningin plants. Therefore, in the CCD8-RNAi potato plants, the lowerstrigolactone content has likely disrupted this mechanism resultingin a redirection of resources away from the belowground axillarybuds.

Interestingly,many of the stolons that formon theCCD8-RNAiplants tend to emerge aboveground and become highly branched,suggesting that once formed, plant resource availability to thestolons is not restricted. The lower number, and typically smallersize of the potato tubers on the CCD8-RNAi plants is reminiscentof the recently reported fewer and smaller fruit phenotype of thetomato CCD8-RNAi plants (Kohlen et al., 2012). However, moreresearch is needed to confirm whether the phenotypes of thestrigolactone-depleted plants are due to the ability of strigolactonesto affect resource partitioning directly (e.g. by modulating sinkstrength, resource transport, etc.; Bennett et al., 2012) or indirectly

(e.g. modulating the growth of one tissue alters resource availabilityto other tissues).

Concluding comments

It has been < 5 yr since strigolactones were identified as a new classof plant hormone that regulate shoot branching. Strigolactones arenow known to modify many plant traits that are of greatimportance to agricultural and horticultural industries including:adventitious rooting, wood formation, branching and crop yieldand quality. The information we have now gives us a tantalizingglimpse into the function(s) of strigolactones but more research isneeded to clarify the mechanisms through which they elicit theireffects.

Acknowledgements

The author would like to thank both Professor Christine Beveridgeand Dr Phillip Brewer for critically reviewing the manuscript andproviding insightful comments. This commentary was funded bythe Australian Research Council.

Michael Glenn Mason

School of Biological Sciences, The University of Queensland,St Lucia, Queensland, 4072, Australia

(tel +61 7 3365 8821; email Michael.Mason@uq.edu.au)

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Key words: auxin transport, cell cycle, meristem dormancy, resource partitioning,

strigolactone.

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