Environment sensing in spring‐dispersed seeds of a winter annual Arabidopsis influences the regulation of dormancy to align germination potential with seasonal changes

Abstract

Seed dormancy cycling plays a crucial role in the lifecycle timing of many plants. Little is known of how the seeds respond to the soil seed bank environment following dispersal in spring into the short-term seed bank before seedling emergence in autumn.Seeds of the winter annual Arabidopsis ecotype Cvi were buried in field soils in spring and recovered monthly until autumn and their molecular eco-physiological responses were recorded.DOG1 expression is initially low and then increases as dormancy increases. MFT expression is negatively correlated with germination potential. Abscisic acid (ABA) and gibberellin (GA) signalling responds rapidly following burial and adjusts to the seasonal change in soil temperature. Collectively these changes align germination potential with the optimum climate space for seedling emergence.Seeds naturally dispersed to the soil in spring enter a shallow dormancy cycle dominated by spatial sensing that adjusts germination potential to the maximum when soil environment is most favourable for germination and seedling emergence upon soil disturbance. This behaviour differs subtly from that of seeds overwintered in the soil seed bank to spread the period of potential germination in the seed population (existing seed bank and newly dispersed). As soil temperature declines in autumn, deep dormancy is re-imposed as seeds become part of the persistent seed bank.

Genetic Variation for Thermotolerance in Lettuce Seed Germination Is Associated with Temperature-Sensitive Regulation of ETHYLENE RESPONSE FACTOR1 (ERF1)

“…Temperature is a critical environmental regulator of seed dormancy, signaling seasonal information to seeds to match their germination potential to periods favorable for seedling emergence and survival as well as influencing subsequent phases of the plant life cycle (Footitt et al, 2014;Batlla and Benech-Arnold, 2015;Burghardt et al, 2015;Huo and Bradford, 2015). In many crops, domestication has largely eliminated these natural dormancy mechanisms, but in others, such as lettuce, they persist and can cause problems for germination and synchronous crop establishment when temperatures exceed permissive limits .…”

Contrasting germination responses to vegetative canopies experienced in pre- vs. post-dispersal environments

“…Dormancy prevents germination under ephemeral conditions that would stimulate germination in non-dormant seeds, thereby synchronizing non-dormancy with the appropriate germination season (Bewley, 1997;FinchSavage and Leubner-Metzger, 2006;Baskin and Baskin, 2014;Footitt et al, 2014). Seeds that must lose dormancy over time (after-ripen) would require more 'lag time' between the perception of cues during maturation and responses to those cues during germination (DeWitt et al, 1998), which could reduce the accuracy of pre-dispersal cues in predicting seedling performance.…”

“…In species with non-deep physiological dormancy, seeds that lose dormancy during after-ripening may be induced into secondary dormancy if germination requirements are not met, which allows seeds to delay germination until the next favourable season (Bewley and Black, 1994;Baskin and Baskin, 2014;Footitt et al, 2014;Auge et al, 2015). Such additional delays of germination through secondary dormancy induction may further reduce the accuracy with which the maturation environment can predict the seedling environment.…”

Seed dormancy is a dynamic state: variable responses to pre- and post-shedding environmental signals in seeds of contrastingArabidopsisecotypes

“…This takes the form of sensing the maternal environment (light, nitrate and temperature) (Sawhney et al, 1985;Alboresi et al, 2005;Kendall et al, 2011;Kendall and Penfield, 2012;Penfield and Springthorpe, 2012;He et al, 2014;Huang et al, 2014) and the environment of the soil seed bank (light, nitrate and temperature) (Footitt et al, 2011(Footitt et al, , 2013Finch-Savage and Footitt, 2012;Penfield and Springthorpe, 2012). This enables seeds to use environmental signals to determine the time and place of seed germination and subsequent seedling emergence (Baskin and Baskin, 1998;Finch-Savage and LeubnerMetzger, 2006;Footitt et al, 2011Footitt et al, , 2013Footitt et al, , 2014. Within a species, the initial depth of primary dormancy is determined during seed development by ecotype genetics and the prevailing environment (Baskin and Baskin, 1998;Kendall et al, 2011;Donohue, 2014;He et al, 2014;Huang et al, 2014).…”