Plant biology

LURE is bait for multiple receptors

In flowering plants, sperm-containing pollen tubes are guided towards ovules by attractants from the female reproductive organ. Receptors for the attractant molecule AtLURE1 have now been found. See Letters p.241 & p.245

For flowering plants to achieve fertilization, pollen must transport sperm across long distances. Sperm-containing pollen grains land on the stigma of the female reproductive organ (the pistil), but the female gametophyte structures that bear eggs are located in distant ovules, so each grain produces a pollen tube that grows towards them1 (Fig. 1a). How pollen tubes find their target has long puzzled biologists. The female gametophyte is known to produce chemoattractant molecules, such as cysteine-rich peptides called LUREs1,2, but the identity of their receptors on pollen tubes has been unclear. Two papers in this issue3,4 identify several molecules on the cell membrane that are involved in sensing one such attractant — AtLURE1 — in the model plant Arabidopsis thaliana5. These discoveries underscore the molecular complexity of this male–female communication process, and provide a foundation for understanding the mechanism by which pollen tubes sense attractants.

Figure 1: Long journey for pollen grains.
figure1

a, In flowering plants, sperm-containing pollen grains land on the receptive stigma of the female reproductive organ (the pistil), and form pollen tubes that grow towards egg-bearing structures called female gametophytes, which are located in ovules. Paired synergid cells in the female gametophyte release molecules such as AtLURE1 that attract the tubes. When the pollen tube penetrates a synergid, it ruptures, releasing two sperm for fertilization. b, Wang et al.3 and Takeuchi and Higashiyama4 have identified receptor-like kinase (RLK) proteins on pollen tubes that are involved in ovule targeting. Wang et al. showed that AtLURE1 binds the RLKs MIK1 and MDIS1, promoting their dimerization and inducing MIK1 to add phosphate groups (P) to itself and to MDIS1. Takeuchi and Higashiyama showed that the RLK PRK6 interacts with itself and PRK3, and with guanine-exchange factors (GEFs) that activate Rho GTPase proteins from plants (ROPs), leading to ovule targeting.

It is well established that pollen-specific receptor-like kinase (RLK) proteins can regulate the growth of pollen tubes6. These proteins typically have three domains: an ectodomain that interacts with extracellular signal molecules; a membrane-spanning domain; and a cytoplasmic domain that attaches phosphate groups to target molecules, inducing cellular responses to incoming signals (Fig. 1b). Using different genetic strategies and starting from an overlapping list of almost 30 pollen-expressed RLKs, the two groups searched for proteins that support ovule targeting by pollen tubes.

On page 241, Wang and colleagues3 report two pairs of closely related RLKs. The authors named the first pair male discoverer 1 (MDIS1) and MDIS2, and the second pair MDIS1-interacting RLK 1 (MIK1) and MIK2. Mutation in the genes that encode each of these four RLKs compromised ovule targeting, and further genetic analysis suggested that MDIS1 and MIK1 act in the same pathway. Next, the authors performed attractant assays in a 'semi in vivo' system, in which pollen tubes are first allowed to grow through the pistil, which primes them to respond to attractants2,5 when subsequently placed under in vitro growth conditions. The assay confirmed that mutations in the MDIS1, MIK1 and MIK2 genes impair the ability of pollen tubes to target AtLURE1, although each mutation suppressed targeting only moderately.

Using similar assays, Takeuchi and Higashiyama4 (page 245) identified another set of RLK receptors for AtLURE1. One, named pollen-specific receptor kinase 6 (PRK6), was essential for pollen tubes to target AtLURE1 in the semi in vivo assay. However, in the pistil, PRK6 mutant pollen tubes displayed only moderate defects in growth and ovule targeting. When the authors combined PRK6 mutations with mutations in the related genes PRK1, PRK3 and PRK8, pollen tubes displayed more-severe guidance defects, including failure to enter ovules.

The attractants identified so far show species specificity1,2. Both Wang et al. and Takeuchi and Higashiyama showed that they could significantly enhance the ability of pollen tubes from a relative of Arabidopsis, Capsella rubella, to target A. thaliana AtLURE1, by engineering them to express MDIS1 or PRK6, respectively — experiments that further support the role of these RLKs in attractant sensing. Taken together, the groups' results indicate that the perception system for AtLURE1 involves multiple RLKs that are functionally redundant, acting together to support ovule targeting by pollen tubes and ensure reproductive success.

Wang et al. provided biochemical and biophysical data to demonstrate a physical and functional interaction between their two pairs of RLKs, and to show that AtLURE1 affects the RLKs' interaction and binds directly to MDIS1, MIK1 and MIK2 with different affinities. Technical difficulties that arose owing to a lack of binding specificity prevented Takeuchi and Higashiyama from reporting similar AtLURE1–PRK interaction experiments, although Wang et al. demonstrated that AtLURE1 did not bind appreciably to PRK3 in a test that they did to demonstrate the specificity of AtLURE1 for their RLKs. These differences might be due to variations in protein preparation and quality, or assay conditions, between the two groups; they will need to be resolved.

Using leaf-cell-based assays, both studies next investigated the mechanisms that mediate AtLURE1 signalling (Fig. 1b). Takeuchi and Higashiyama showed that PRK3 and PRK6 interact with guanine-exchange factors that activate Rho GTPase proteins, affirming a known link between PRK proteins and these signal mediators6. How AtLURE1 affects these interactions remains to be shown. Wang et al. found that AtLURE1 induces MDIS1–MIK1 binding and promotes phosphorylation of the two RLKs by MIK1, implying that changes in the phosphorylation states of these kinases underlie their ability to transform the attractant signal into a guidance response. Future experiments should confirm these interactions in pollen tubes, and test whether these pathways intersect as segments of the same AtLURE1-triggered cascade.

Finally, both groups showed that the location of their RLKs was altered by AtLURE1, bolstering the assertion that these are bona fide AtLURE1 receptors. Wang et al. reported that AtLURE1 induced the removal of MDIS1 from the cell membrane — a change that implies a receptor response to binding. Takeuchi and Higashiyama demonstrated that AtLURE1 altered the distribution of PRK6 around the apex of the pollen tube such that it concentrated on tube surfaces closer to the attractant, correlating receptor localization with a change in growth direction.

RLKs have crucial roles in plant development, reproduction and responses to environmental challenges. These studies now persuasively establish that RLKs are involved in attractant-sensing by pollen tubes. Moreover, they support the idea that functional redundancy between receptors — and between attractants, as previously suggested2,5 — is perhaps genetically hardwired to ensure reproductive success.

However, this redundancy raises a perplexing question about how AtLURE1 differentiates between potential targets. To capitalize on redundant receptors, AtLURE1 has apparently evolved to interact with a range of RLKs, even those with other specialized functions. For instance, Wang et al. found that AtLURE1 binds PXY, a close relative of MIK1 that controls vascular differentiation7, with an affinity comparable to that for MIK1. However, an attractant closely related to AtLURE1 does not seem3,8 to interact with an RLK called ERECTA that controls plant architecture and cell shape at the leaf surface. Clearly, there is a need to determine how cysteine-rich peptide attractants such as LUREs identify the receptors capable of mediating ovule targeting. It will also be interesting to investigate the possibility of functional crossover by other pairs of RLK and growth regulators, including PXY and ERECTA and their interaction partners, if they are expressed in regions close to where male–female communication occurs.

The arsenal of signalling molecules in plants — in particular peptide signal molecules9 and RLKs4,5 — is immense. It will not be surprising if more attractant–receptor pairs are discovered. The current studies, together with our knowledge of other growth regulatory molecules that interact with pollen tubes before they encounter ovule attractants10, bring us closer to fully understanding a process that is vital for plant reproduction.Footnote 1

Notes

  1. 1.

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Correspondence to Alice Y. Cheung or Hen-Ming Wu.

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Cheung, A., Wu, H. LURE is bait for multiple receptors. Nature 531, 178–180 (2016). https://doi.org/10.1038/531178a

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