Emerging trends in strigolactone research
(tel +61 7 3365 8821; Michael.Mason@uq.edu.au)
In 2008, back-to-back publications in the journal Nature revealed that strigolactones are a new class of plant hormones that control shoot architecture by inhibiting axillary bud growth (Gomez-Roldan et al., 2008; Umehara et al., 2008). Since then, strigolactones have been established as an important group of plant growth regulators that affect a raft of different plant processes (see review Brewer et al., 2013). In this issue of New Phytologist, a surprising new role of strigolactones in stolon and tuber development is revealed by Pasare et al. (pp. 1108–1120) that adds support to emerging theories of strigolactone involvement in resource partitioning.
‘Why then do the strigolactone-deficient CCD8-RNAi plants have less, not more, stolons?'
Pasare et al. used RNAi technology to generate potato plants with reduced expression of CCD8, a key gene in the strigolactone biosynthesis pathway. The resultant plants had significantly reduced strigolactone content and displayed many of the traits observed in other strigolactone-deficient plants, such as increased axillary shoot branching and decreased plant height. However, the most intriguing discovery is the effect of strigolactone deficiency on stolon (underground stem) development; the CCD8-RNAi plants had reduced stolon formation, with typically fewer and smaller tubers. Strigolactone deficiency also had a dramatic effect on the growth habit of the stolons such that the majority of the stolons showed a loss of diageotropic growth pattern, emerging aboveground instead of growing horizontally outwards into the soil.
These discoveries are important on a number of levels; first, these findings have large implications for improving the pre- and post-harvest traits of the potato, which will likely have many beneficial flow-on effects for the economically important potato industries around the world. Second, from a biology perspective, every new plant process that strigolactones are found to regulate brings us a step closer to understanding the mechanism(s) of strigolactone function. To date, we still know very little about how strigolactones elicit their effects on plant development; however, evidence is starting to emerge that indicates that strigolactones appear to function by modulating auxin transport, cell division/meristem dormancy, and resource partitioning. These are not mutually exclusive and, in fact, it is likely that each strigolactone-regulated process involves a combination of two, or all three of these mechanisms.
Strigolactones modulate auxin transport
Plants with defects in strigolactone synthesis have been found to have higher rates of auxin movement through the polar auxin transport stream (Brewer et al., 2009; Shinohara et al., 2013). The higher auxin transport rate appears to be due to increased levels of the 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 dependent manner. Recently, it was revealed that GR24 is able to reduce auxin transport by rapidly promoting endocytosis of PIN1 (Shinohara et al., 2013). With less PIN1 on the plasma membrane, the rate at which auxin can be transported out of the cell decreases.
The effect of strigolactones on PIN1 has led some researchers to hypothesize that by inhibiting auxin transport out of buds, strigolactones are able to prevent axillary bud outgrowth (Shinohara et al., 2013). However, a number of studies have now revealed that the relationship between polar auxin transport and axillary bud outgrowth is more complicated than first thought (Ferguson & Beveridge, 2009). For example, disruption to auxin transport by stem girdling or chemical treatment does not always correlate with axillary bud outgrowth, indicating that there are likely other, as yet, unknown mechanisms that are also important for apical dominance. Moreover, chemically reducing the rate of auxin transport in the strigolactone mutants to wild-type levels results in only a partial restoration of their branching phenotype (Bennett et al., 2006). These results indicate that modifying auxin transport is only one of the mechanisms employed by strigolactones to inhibit axillary bud growth.
Strigolactones regulate cell division/meristem dormancy
The ability of strigolactones to limit adventitious rooting by inhibiting the initial formative divisions of the founder cells (Rasmussen et al., 2012) indicates that strigolactones may be able to regulate cell division in specific tissues within the plant. Consistent with this, strigolactones have been found to induce cell division in interfascicular cambium tissues within plant stems (Agusti et al., 2011). Furthermore, in axillary buds, strigolactones promote the expression of BRANCHED1 (BRC1), a key transcriptional regulator of bud dormancy that is thought to be involved in the maintenance of the stem cell niche, cell division, and lateral organ initiation (Dun et al., 2012). These results indicate that one of the functions of strigolactones is to modulate cell division and meristem dormancy in specific tissues.
Interestingly, cytokinin inhibits the expression of BRC1 and a combination of strigolactone and cytokinin results in intermediate expression (Dun et al., 2012). Bud outgrowth appears to be determined by the ratio of strigolactone to cytokinin in buds which act, at least in part, through BRC1. BRC1 is not the only common target of these two hormones; cytokinin, like strigolactone, also regulates auxin transport by promoting PIN1 removal from the plasma membrane (Marhavy et al., 2011). These results indicate that one of strigolactone's mechanisms of action may be to modulate cytokinin action through common targets. It remains to be determined whether strigolactones can also target the same genes through which cytokinins regulate the cell cycle (Hwang et al., 2012).
Strigolactones modulates resource partitioning in plants
It is now becoming apparent that strigolactones play an important role in maintaining phosphate and nitrogen homeostasis in plants. Consistent with previous findings (Yoneyama et al., 2007), Pasare et al. report that strigolactone levels significantly increase under phosphate-limiting conditions. A likely reason for this rise in strigolactone in some plant species is to enhance the association with arbuscular mycorrhizal fungi in order to improve phosphate uptake from the rhizosphere. Additionally, the ability of strigolactones to modify plant growth (e.g. shoot branching, lateral root initiation, root hair production; Koltai, 2011) supports a role for strigolactones in regulating the flow of plant resources towards specific 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 for strigolactones in regulating resource allocation. The finding that the CCD8-RNAi plants have decreased stolon formation is intriguing given that stolons are stem branches that originate from axillary buds towards the base of the main stem. Why then do the strigolactone-deficient CCD8-RNAi plants have less, not more, stolons? In strigolactone-deficient pea plants, not all axillary buds grow out and the pattern of bud outgrowth is influenced by environmental conditions (Beveridge et al., 2003). These results indicate the possibility that additional signals may act through, or in conjunction with strigolactones to regulate resource partitioning in plants. Therefore, in the CCD8-RNAi potato plants, the lower strigolactone content has likely disrupted this mechanism resulting in a redirection of resources away from the belowground axillary buds.
Interestingly, many of the stolons that form on the CCD8-RNAi plants tend to emerge aboveground and become highly branched, suggesting that once formed, plant resource availability to the stolons is not restricted. The lower number, and typically smaller size of the potato tubers on the CCD8-RNAi plants is reminiscent of the recently reported fewer and smaller fruit phenotype of the tomato CCD8-RNAi plants (Kohlen et al., 2012). However, more research is needed to confirm whether the phenotypes of the strigolactone-depleted plants are due to the ability of strigolactones to affect resource partitioning directly (e.g. by modulating sink strength, resource transport, etc.; Bennett et al., 2012) or indirectly (e.g. modulating the growth of one tissue alters resource availability to other tissues).
It has been < 5 yr since strigolactones were identified as a new class of plant hormone that regulate shoot branching. Strigolactones are now known to modify many plant traits that are of great importance to agricultural and horticultural industries including: adventitious rooting, wood formation, branching and crop yield and quality. The information we have now gives us a tantalizing glimpse into the function(s) of strigolactones but more research is needed to clarify the mechanisms through which they elicit their effects.
The author would like to thank both Professor Christine Beveridge and Dr Phillip Brewer for critically reviewing the manuscript and providing insightful comments. This commentary was funded by the Australian Research Council.