[Nature] FERONIA controls pectin- and nitric oxide-mediated male–female interaction
The FER-mediated presence of de-esterified pectin underlies prevention of the entrance of supernumerary pollen tubes into ovules.
[Nature. 2020 Mar;579:561-566]
Abstract
Species that propagate by sexual reproduction actively guard against the fertilization of an egg by multiple sperm (polyspermy). Flowering plants rely on pollen tubes to transport their immotile sperm to fertilize the female gametophytes inside ovules. In Arabidopsis, pollen tubes are guided by cysteine-rich chemoattractants to target the female gametophyte1,2. The FERONIA receptor kinase has a dual role in ensuring sperm delivery and blocking polyspermy3. It has previously been reported that FERONIA generates a female gametophyte environment that is required for sperm release4. Here we show that FERONIA controls several functionally linked conditions to prevent the penetration of female gametophytes by multiple pollen tubes in Arabidopsis. We demonstrate that FERONIA is crucial for maintaining de-esterified pectin at the filiform apparatus, a region of the cell wall at the entrance to the female gametophyte. Pollen tube arrival at the ovule triggers the accumulation of nitric oxide at the filiform apparatus in a process that is dependent on FERONIA and mediated by de-esterified pectin. Nitric oxide nitrosates both precursor and mature forms of the chemoattractant LURE11, respectively blocking its secretion and interaction with its receptor, to suppress pollen tube attraction. Our results elucidate a mechanism controlled by FERONIA in which the arrival of the first pollen tube alters ovular conditions to disengage pollen tube attraction and prevent the approach and penetration of the female gametophyte by late-arriving pollen tubes, thus averting polyspermy.
- The FER-mediated presence of de-esterified pectin underlies prevention of the entrance of supernumerary pollen tubes into ovules.
- Pollination induces FER-dependent NO at the filiform apparatus.
- Pollinated pistil exudates and de-esterified pectin fragments induce FER-dependent NO.
- NO affects LURE1 and suppresses pollen tube attraction.
Summary
The diagram summarizes previously published results on how FER mediates pollen tube rupture and sperm release to enable fertilization (steps 2 and 3 in the scheme), and results reported here on how FER affects two interconnected conditions at the filiform apparatus to prevent the penetration of ovules by supernumerary pollen tubes (steps 4 and 5 in the scheme). Solid lines reflect information that comes directly from experimental data; dashed lines reflect extrapolations from experimental data and other relevant information. Results present in this Article show that FER maintains a pistillate environment enriched in de-esterified pectin (Fig. 3a) (step 1 in the scheme), including at the filiform apparatus of the female gametophyte (Fig. 1e, f). Pollen tubes are attracted by female guidance cues to depart from their main growth axis to approach ovules, and are then guided by synergid-cell-produced chemoattractants (for example, LUREs) to the ovules to penetrate the female gametophyte.