Anchorage by seed mucilage prevents seed dislodgement in high surface flow: a mechanistic investigation

Abstract

Seed mucilage is a common and highly diverse trait shared among thousands of angiosperms. While long recognized that mucilage allows seeds to anchor to substrates (antitelechory), we still lack a mechanistic understanding of this process. We propose a mechanistic model of how mucilage affects substrate anchorage and fluid resistance, ultimately contributing to antitelechory. To test this model, we subjected mucilaginous seeds of 52 species, varying in eight measured seed traits, to a week of continuous water flow at a range of erosion potentials. Supporting our model, mucilage mass increased both dry and wet attachment strength, which explained time to erosion well. A standard deviation increase in log mucilage mass increased seed time to dislodgement by 280 times. Fluid resistance was largely dependent on speed of water flow and the seed's modified drag coefficient, but not the quality of the seed or seed mucilage. Neither mucilage expansion speed nor mucilage decay rate explained dislodgement potential well. Our results suggest that the high substrate anchorage strength is the primary role of mucilage in fostering seed establishment in highly erosive environments. In contrast, other seed and mucilage trait differences among species are of lesser importance to antitelechory.

Rain events at maturity severely impact the seed quality of psyllium (Plantago ovata Forssk.)

“…We have observed microbial overgrowth on non-disinfested seeds to significantly reduce seedling establishment under non-sterile conditions in pot experiments and in the field. Furthermore, mucilage has been implicated in successful establishment, especially under adverse conditions, in many mucilageproducing species (Pan et al, 2021;Pan et al, 2022;Tsai et al, 2021;Yang et al, 2012) including Plantago (Pan et al, 2021(Pan et al, , 2022Teixeira et al, 2020;Veiga-Barbosa & Pérez-García, 2014;Zhang et al, 2014). It is possible that changes to the mucilage in rain-damaged seeds will also contribute to reduced establishment in the field and thus trials should be conducted to determine if rain-damaged seeds are at all suitable for resowing.…”

Drying conditions alter the defensive function of seed mucilage against granivores

“…However, we have a strong mechanistic hypothesis integrating these results and previous research. In interspecific comparisons of over fifty species, attachment strength was strongly correlated with mucilage volume (Pan et al 2021(Pan et al , 2022. Mucilage volume probably affects attachment strength by altering the area of contact (hypothesized in Grubert 1974); therefore, it is likely that the rapid decline in volume at higher temperatures or at low humidity simply led to a smaller area of substrate that the mucilage strands were in contact with; it is likely that the reduced attachment strength in several species in the refrigerator treatment was due to the humidity control in household refrigerators.…”

“…Coupled with the findings in this study of stronger attachment at lower drying temperatures, we think it is reasonable to assume that species or populations regularly experiencing higher temperatures may need greater attachment strength to obtain the same protection that may come with the rapid drying in warmer areas. Therefore, we believe that in addition to the environment modifying the function of mucilage, it also likely is a potent selective force that may, in part, drive the diversity of mucilage properties we see across plants (Grubert 1974, Western 2012, LoPresti et al 2019, Cowley et al 2021Pan et al 2021Pan et al , 2022.…”

“…While differences in attachment strength are likely to drive differential survival between seeds, it is likely that mucilage volume, as the underlying trait strongly correlating with force needed to dislodge the seed (Pan et al 2021(Pan et al , 2022 is the heritable component that selection would act on. 2) The interplay between attachment strength and area of attachment, with consideration of both mucilage volume and seed shape (i.e., the flat seeds of flax versus the nearly spherical seeds of chia).…”

“…These seeds are unassuming and entirely nonsticky when dry, yet when wetted, the polysaccharide coating swells into a viscid mass (Figure 1, top row); when dried again, the mucilage strands strongly cement the seed to whatever it is in contact with (Figure 1, middle row). This attachment defends the seed from small granivores (Pan et al 2021), sticks to animals for dispersal (Rønsted et al, 2002), and protects the seed from dislodgement (Pan et al 2022), as well as ameliorating the effects of harsh germination environments (Teixiera et al 2020). The chemical composition, volume, structure, and physical properties of the mucilage layer vary greatly across species (Western 2012, Phan et al 2018, Kreitschitz et al 2021a.…”