10th World Congress on Parasitic Plants, Kusadasi, Turkey, June 2009
Parasitic plants can exhibit such unusual biology that they sometimes have not even been recognized as plants. Such was the report of Jay Bolin (Old Dominion University, Norfolk, VA, USA), at the recent gathering of the International Parasitic Plant Society in Kusadasi, in his recounting of the first descriptions of holoparasitic species in the Hydnoraceae family. Although there were plenty of presentations highlighting the specialized anatomy and communication exhibited by parasitic plants, this meeting was marked by an increasing sense of the common themes shared between parasitic plants and other plant species. In one example, Marc-André Selosse (CNRS, Montpellier, France) described striking parallels between parasitic plants and mycoheterotrophic and mixotrophic species that dine on fungi (Selosse & Roy, 2009). Also, as described later, the signaling molecule detected by some parasitic plants to locate their hosts has turned out to be a new plant hormone. This report will focus on research of broader interest to plant scientists; so many excellent presentations cannot be included. Nevertheless, it is noteworthy that the parasitic plant congresses are characterized by all manner of diversity. Over 100 participants represented 37 different countries from around the globe and the presentations described work on dozens of parasitic species. Every aspect of parasitic plant biology was under consideration, including ecology, evolution, population biology, biochemistry, physiology, and interactions with hosts and pathogens. The conservation of rare parasitic species was discussed, but a larger number of presentations focused on control of weedy species of the genera Striga and Orobanche, which decimate crops across Africa, the Mediterranean and the Middle East regions. Taxonomy was also on the agenda, and Danny Joel (Agricultural Research Organization, New Ya'ar, Israel) reviewed the evidence for renaming several Orobanche species to Phelipanche. Although there was no consensus for immediately adopting the name change, the use of both names in the literature is already reaching the point that researchers would be wise to use both names in keyword searches.
‘…an intriguing question is whether Striga and Orobanche produce their own strigolactones: if not, how do they control branching; if yes, how can they still respond in such a sensitive manner to strigolactones of hosts’ root exudates?’
The life-or-death decision to germinate
An important step in the life cycle of all obligate parasitic plants is their germination in the right place and at the right time, enabling them to establish the connection they require to survive. The root parasitic Orobanche and Striga spp. use the so-called germination stimulants – secreted by the roots of their hosts – to achieve this. The best studied class of these stimulants is the strigolactones. Ground-breaking work of Koichi Yoneyama et al. (Utsunomiya University, Utsunomiya, Japan) on the analysis of strigolactones in the root exudate of many plant species has opened up possibilities to study their importance and regulation in greater detail.
Kaori Yoneyama (Teikyo University, Utsunomiya, Japan) showed that there is substantial genetic variation in the strigolactone profile exuded by maize varieties. Moreover, she was able to correlate the composition of the exudate to the resistance/susceptibility towards Striga. Also in rice, there is a substantial genetic variation in strigolactone production, with concentrations in the exudate differing by 100-fold or more between varieties, as presented by Muhammad Jamil (Wageningen University, Wageningen, the Netherlands). Both reports have important implications for resistance breeding as genetic variation allows for selection to improve Striga resistance.
This raises the important issue of host specificity, which may be influenced from two sides: the sensitivity of (species or ecotypes or races of) the parasite for different germination stimulants; and/or the production of different mixtures of germination stimulants by different hosts (species and varieties). Anna Hoeniges (‘Vasile Goldis’ Western University, Arad, Romania) compared the strigolactone production of a number of hosts of weedy and nonweedy broomrapes, postulating how host specificity (or the lack thereof) has arisen in several Orobanche spp. The efforts to identify the strigolactone receptor in Orobanche and Striga that were briefly mentioned by Harro Bouwmeester (Wageningen University, Wageningen, the Netherlands) will hopefully help to shed more light on the mechanism of host specificity.
With regard to parasitic weed control, interesting new results were presented in relation to the germination stimulants. Tadao Asami et al. (University of Tokyo, Japan) presented a poster detailing the synthesis of strigolactone biosynthesis inhibitors with the objective of blocking germination stimulant production by crops to make these crops less susceptible to Striga or Orobanche. Of course, it is also of great interest for scientific purposes to have such selective inhibitors. In a similar vein, the long-known fact that increased fertilization leads to Striga suppression was explained in presentations by Muhammad Jamil (Wageningen University, Wageningen, the Netherlands) and Kaori Yoneyama (Teikyo University, Utsunomiya, Japan), reporting a strong negative correlation between the amount of nitrogen and/or phosphate application and the concentration of strigolactones in the exudate of rice. These concentration differences correlated well with Striga performance: the lower the nutrient availability, the higher the germination-inducing capacity of the exudate and the more Striga attachment/emergence in a pot experiment.
Do parasitic plants have a hormone problem?
One of the most exciting discoveries of the last year was the fact that strigolactones were shown to be a new class of plant hormones (Gomez-Roldan et al., 2008; Umehara et al., 2008). This was the second surprise about strigolactones in recent years, with Akiyama et al. discovering, in 2005, that the strigolactones are – in addition to germination stimulants for root parasitic plants – also host-finding factors for the symbiotic arbuscular mycorrhizal fungi (Akiyama et al., 2005).
Several of the co-authors contributing to the discovery of the hormonal function of the strigolactones (Koichi Yoneyama, Utsonomiya University, Utsunomiya, Japan; Satoko Yoshida, RIKEN, Yokehama, Japan; and Harro Bouwmeester, University of Wageningen, Wageningen, the Netherlands) attended the meeting. Harro presented a review of this exciting development, explaining how it was enabled by the discovery that the strigolactones are biosynthetically derived from the carotenoids through the action of a carotenoid-cleaving enzyme (Matusova et al., 2005). The search for mutants in such enzymes quickly resulted in the discovery that some ramosus (rms) mutants in pea and dwarf (d) mutants in rice, which are mutated in a CCD7 or a CCD8 enzyme, do not produce detectable amounts of strigolactones. Also in Arabidopsis, bioassays with Orobanche or Striga seeds suggest that the more axillary branching (max) mutants, max3 and max4 (mutated in a CCD7 or a CCD8 enzyme, respectively) do not produce strigolactones.
However, as the names of these mutants suggest, they exhibit a morphological phenotype: abnormally high branching (pea, Arabidopsis) or high tillering (rice) (Fig. 1). The mutants could be restored to the wild-type phenotype by the application of the synthetic strigolactone, GR24, showing that strigolactones (or a close derivative thereof) represent the so-called branching inhibiting signal (BIS) that was postulated to exist many years before (Booker et al., 2004).
Exciting opportunities for parasitic plant research that arise from this discovery are the fact that there are a number of other rms, d (or high-tillering dwarf (htd )) and max mutants available. The Arabidopsis max1 mutant, for example, has a mutation in a cytochrome P450, yet the branched phenotype of this mutant and the genetic evidence suggests that the mutant is not making the BIS. With regard to perception of the strigolactones, the d3, max2 and rms4 mutants are of particular interest. These mutants do make BIS but do not perceive it, resulting in the branched/tillered phenotype, which cannot be restored to the wild-type phenotype. These mutants are deficient in an F-Box receptor-like protein that is similar to transport inhibitor response 1 (TIR1), a protein involved in auxin perception/signal transduction. The fact that this F-Box protein is involved in the perception of the BIS in plants makes it a good candidate for the perception of strigolactones in Orobanche and Striga seeds. Harro Bouwmeester (University of Wageningen, Wageningen, the Netherlands) showed preliminary results of binding studies with biotinylated-GR24 to MAX2, which were carried out in collaboration with Binne Zwanenburg (University of Nijmegen, Nijmegen, the Netherlands) and Ottoline Leyser (University of York, UK).
Considering that the strigolactones seem ubiquitous in the plant kingdom, an intriguing question is whether Striga and Orobanche produce their own strigolactones: if not, how do they control branching; if yes, how can they still respond in such a sensitive manner to strigolactones of hosts’ root exudates? Undoubtedly, this will be an area of great interest for the parasitic plant community in the next couple of years.
Parasitic plants join the genomics club
While genomic resources have been amassed for model plants and major crops over the past decade, few gene sequences have been available for parasites. This situation is now changing as at least two projects are poised to release substantial amounts of parasite sequence data. Jim Westwood (Virginia Tech, Blacksburg, VA, USA) and Claude dePamphilis (Penn State University, State College, PA, USA) described a project funded by the US National Science Foundation that is in the process of sequencing expressed sequence tags (ESTs) from several key stages of the life cycles of three species: Triphysaria versicolor, Striga hermonthica and Orobanche (syn. Phelipanche) aegyptiaca. These members of the family Orobanchaceae span the continuum from facultative parasite to achlorophyllous holoparasite and provide a framework for understanding the evolution of parasitism. The first sets of genes produced by this project comprise approximately 31 000 unigenes from shoots of S. hermonthica and 24 000 unigenes from pre-emerged tissues of O. aegyptiaca. In a separate project, Satoko Yoshida (RIKEN, Yokehama, Japan) reported the pending public release of 17 000 unigenes derived from multiple stages of S. hermonthica. Although a substantial data set of haustorial development-related genes for T. versicolor has been available for a few years (Torres et al., 2005), this new influx marks a milestone in parasitic plant research.
The immediate impact of new parasite sequences will probably be felt by researchers working on parasite biochemistry, physiology and host–parasite communication. This includes the work on seed germination described earlier, as well as studies, such as that being conducted by Thomas Péron (University of Nantes, Nantes, France) to understand how the parasite uses vacuolar invertase and sucrose synthase to maintain strong sink strength relative to its host. Studies of host resistance have already harnessed host genomic resources to describe global gene expression in response to parasitism (Karolina Lis, University of Virginia, Charlottesville, VA, USA) and identified new resistance mechanisms (Kan Huang, University of Virginia, Charlottesville, VA, USA; Grégory Montiel, University of Nantes, Nantes, France), but having parasite sequences will enable even more sophisticated understanding of the host–parasite interaction.
The trickle of parasite sequence data is now a stream and will probably soon become a flood as additional sequences become available from Striga, Orobanche and other parasitic species. This will provide abundant opportunities for comparing gene structure and function across plants exhibiting a great diversity of morphologies. This should be of interest to a wide variety of plant scientists who would like to know how their favorite gene has been modified in a parasitic plant lineage.