Pollen wall degradation in the Brassicaceae permits cell emergence after pollination

Abstract

PREMISE OF THE STUDY: Despite attempts to degrade the sporopollenin in pollen walls, this material has withstood a hundred years of experimental treatments and thousands of years of environmental attack in insects and soil. We present evidence that sporopollenin, nonetheless, locally degrades only minutes after pollination in Arabidopsis thaliana flowers, and describe here a two‐part pollen germination mechanism in A. thaliana involving both chemical weakening of the exine wall and swelling of the underlying intine. METHODS: We explored naturally occurring components from pollen and stigma surfaces and found a tripartite mix of hydrogen peroxide, peroxidase and catalase enzymes (all at high levels at the pollination interface) to be experimentally sufficient to degrade the sporopollenin of some Brassicaceae family members. KEY RESULTS: At pollination, factors carried on the pollen surface may mix with factors on the stigma surface in a reaction that locally oxidizes the exine pollen wall. Hydrogen peroxide, catalases, and peroxidases are biologically present at the right time and place and, when mixed experimentally, are sufficient to degrade the walls of susceptible pollen. CONCLUSIONS: Our work on native biochemistry for breaching sporopollenin suggests new research directions in pollen aperture evolution and could aid efforts to analyze sporopollenin's composition, needed for application of this corrosion‐resistant, but long‐intractable material.

Comprehensive Proteomic Profiling of the Brassica carinata and Triticale Mature Stigma and Pollen

“…al., 2006). In addition, small increases in temperature were observed when stigmas from Arabidopsis were dusted with pollen, which is consistent with catalase's exothermic decomposition of H2O2 (Edlund et. al., 2017).…”

“…This is in agreement with the fact that the receptive stigma needs to be responsive to many different external stimuli in addition to producing many proteins involved in defense for protection against invasive microorganisms that could take advantage of the wound caused by the invading pollen tube. On the other hand, the pollen's highly resistant exine wall acts as a physical and chemical barrier to microbial and insect degradation (Edlund, et. al., 2017) and therefore might not need to have as many proteins readily available for defense or responses to stimuli.…”

“…al., 2012), and locally restricted ROS production at a pollen grain aperture was required for outgrowth at that particular aperture. ROS has also been implicated in pollen exine breach in a two-step process where a swollen intine (due to turgor pressure from hydration) pushes against an exine weakened by redox reactions present at the pollen-stigma interface, resulting in exine rupture at the site of pollen tube emergence (Edlund et. al., 2017).…”

“…The stigma contained a higher proportion of defense response proteins than the pollen (Table S3.4 and S3.5) and one of the uniquely enriched sub-categories was Defense Response to Virus. Since the pollen grain exine wall consists of the highly resistant biopolymer sporopollenin, which can withstand degradation by microbes and insects (Edlund, et. al., 2017), this may explain why proteins involved in the defense response are not as prevalent within the pollen grain as in the stigma.…”

Human blood plasma catalyses the degradation of Lycopodium plant sporoderm microcapsules

“…Although extremely robust, several methods for sporopollenin degradation have been reported, including ozonolysis 37 , acetolysis 38 , photocatalytic reactions 39 and redox reactions with hydrogen peroxide 40 , peroxidase and catalase 40 . However, much of the researches pertain to harsh conditions that bear no correlation to biological systems – a particularly important point for potential biological applications of sporopollenin-based microcapsules such as drug delivery considering its biocompatibility, renewability and low cost.…”