Sensitivity to hypoxia and microbial activity are instrumental in pericarp-imposed dormancy expression in sunflower (Helianthus annuus L.)

Abstract

We used two sunflower genotypes displaying pericarp-imposed dormancy at high incubation temperatures (i.e. 30°C) to investigate the role of the pericarp as a limitation to oxygen availability to the embryo (hypoxia), and its impact on embryo abscisic acid (ABA) content and sensitivity to ABA. Results showed that both genotypes displayed very different oxygen threshold values for inhibition of embryo germination when incubation was performed at 30°C. Expression of dormancy in one genotype was therefore related to exacerbated embryo sensitivity to hypoxia, whereas in the other genotype, the pericarp appeared to act as a more severe restraint to oxygen entry. Increased sensitivity to hypoxia was, in part, related to increased sensitivity to ABA, but not to alterations in ABA metabolism. The activity of pericarp-microbial communities (bacteria and fungi) at high temperatures was also assessed as a potential determinant of hypoxia to the embryo. Oxygen consumption in pericarps incubated at 30°C was attenuated with antibiotics, which concomitantly promoted achene germination. In agreement with the observed more severe oxygen deprivation to the embryo exerted by the pericarp, the bacterial load in the pericarp was significantly higher in the commercial hybrid than in the inbred line; however, the application of antibiotics strongly reduced the bacterial colony counts for each genotype. Different bacterial and fungal communities, assessed through their profiles of carbon-source utilization, were determined between genotypes and after treatment with antibiotics. This work highlights the relationship between enhancement of sensitivity to hypoxia with incubation temperature and seed dormancy expression, and suggests that microbial activity might be part of the mechanism through which hypoxia is imposed.

Dormancy attributes in sunflower achenes (Helianthus annuusL.): I. Intraspecific variability

“…Indeed, seed/embryo responsiveness to ABA was positively linked to achene inhibition of germination as affected by both LTED and TI. Although TI is imposed to the embryo by the fruit coats (and seeds/embryos germinate fully at 30 ˚C, as reported by Dominguez et al, 2019), our data support that TI involves enhanced embryo sensitivity to ABA, as observed in lettuce by Argyris et al (2008). The distinction between embryo dormancy and coat-imposed dormancy seems somewhat artificial in sunflower and may reflect different degrees of embryo responsiveness to endogenous ABA.…”

“…After cultivation in a common garden and phenotyping for dormancy traits, genotypes were separated into functionally relevant dormancy groups. Overall, genotypes were separated into five groups in Experiment II, differing in the level of LTED (lowest in Group 1 and strongest in Group 5) and the presence or absence of a degree of TI (in Groups 4-5) present in other works (Dominguez et al, 2016;Dominguez et al, 2019). Inbred lines B91 and B123 (from the INTA breeding program), previously described as having contrasting dormancy phenotypes (Andrade et al, 2015;Roselló et al, 2016) were assigned by our PCA to both extreme dormancy Groups 1 and 5 in Experiment II, together with inbred lines 561 and HA342, respectively (both from USDA North Dakota; see Table 1) and which can be used as reference genotypes in future dormancy phenotyping studies.…”

“…By contrast, dormancy expression at high temperatures (i.e., 25-30 ˚C) is dependent on the pericarp (the "naked" embryos germinate). This "coat-imposed dormancy" can persist for several months, and in some genotypes, is not completely attenuated during postharvest dry storage (Dominguez et al, 2016;Dominguez et al, 2019). Indeed, in some sunflower genotypes, inhibition of germination at warmer incubation temperatures (≥25 ˚C) meets the definition of thermoinhibition (TI) as proposed by Hills and Van Staden (2003).…”

“…When nondormant, sunflower achenes can fully germinate at incubation temperatures between 5 and 40 ˚C (Corbineau et al, 1990). In cultivated sunflowers, dormancy expression has been reported at low (i.e., 10-15 ˚C;Bodrone et al, 2017), high (above 20-25 ˚C;Dominguez et al, 2019), or at both low and high incubation temperatures (Corbineau et al, 1990). This produces a positive, negative, or bimodal response pattern for germination along the thermal range.…”

Roles of Hardened Husks and Membranes Surrounding Brachypodium hybridum Grains on Germination and Seedling Growth

“…In addition, the presence of the husk around the caryopses of Aegilops kotschyi inhibited germination [9]. Furthermore, in other species of family Asteraceae, the pericarp induced seed dormancy as it acted as a mechanical constrain hampering water uptake in Glebionis coronaria [10] and oxygen availability in Helianthus annuus [11]. In many of the species where germination was inhibited because of husk presence, a significant increase in germination was observed after husk removal.…”