Salt Induces Features of a Dormancy-Like State in Seeds of Eutrema (Thellungiella) salsugineum, a Halophytic Relative of Arabidopsis

Abstract

The salinization of land is a major factor limiting crop production worldwide. Halophytes adapted to high levels of salinity are likely to possess useful genes for improving crop tolerance to salt stress. In addition, halophytes could provide a food source on marginal lands. However, despite halophytes being salt-tolerant plants, the seeds of several halophytic species will not germinate on saline soils. Yet, little is understood regarding biochemical and gene expression changes underlying salt-mediated inhibition of halophyte seed germination. We have used the halophytic Arabidopsis relative model system, Eutrema (Thellungiella) salsugineum to explore salt-mediated inhibition of germination. We show that E. salsugineum seed germination is inhibited by salt to a far greater extent than in Arabidopsis, and that this inhibition is in response to the osmotic component of salt exposure. E. salsugineum seeds remain viable even when germination is completely inhibited, and germination resumes once seeds are transferred to non-saline conditions. Moreover, removal of the seed coat from salt-treated seeds allows embryos to germinate on salt-containing medium. Mobilization of seed storage reserves is restricted in salt-treated seeds, while many germination-associated metabolic changes are arrested or progress to a lower extent. Salt-exposed seeds are further characterized by a reduced GA/ABA ratio and increased expression of the germination repressor genes, RGL2, ABI5, and DOG1. Furthermore, a salt-mediated increase in expression of a LATE EMBRYOGENESIS ABUNDANT gene and accretion of metabolites involved in osmoprotection indicates induction of processes associated with stress tolerance, and accumulation of easily mobilized carbon reserves. Overall, our results suggest that salt inhibits E. salsugineum seed germination by inducing a seed state with molecular features of dormancy while a physical constraint to radicle emergence is provided by the seed coat layers. This seed state could facilitate survival on saline soils until a rain event(s) increases soil water potential indicating favorable conditions for seed germination and establishment of salt-tolerant E. salsugineum seedlings.

High salinity impacts germination of the halophyte Cakile maritima but primes seeds for rapid germination upon stress release

“…The CRB, CRA1, 11S Globulin and pAF7 were especially affected under stress recovery (Figs 3A and 5). Recently, it was also documented (Kazachkova et al 2016) that salinity inhibited germination of the halophyte E. salsugineum by inducing a seed state with molecular traits of dormancy, including retarded and inhibited SSP break down. Yet, strong germination recovery associated with high SSP mobilization was noticed upon stress relief, which is in agreement with our data.…”

“…More generally, this is consistent with other reports highlighting the salt-sensitivity of annual halophytes at the early developmental stages of their ontogeny. For instance, the delayed germination onset was documented for halophytes like Suaeda salsa (Li et al 2015), Plantago coronopus (Bueno et al 2017) and Eutrema salsugineum (Kazachkova et al 2016). In rice, the prolongation of phase II (imbibition) in response to high salinity accounted for the slower germination rate (Xu et al 2017).…”

“…A deep understanding of survival strategies of halophytes in response to salt stress at the germinative and early seedling stages is of paramount importance for breeding salt‐tolerant lines and cultivars and for assessing the potential of various halophytes as crop species (Gul et al 2013). While the physiological basis underlying the salt‐enforced dormancy and seed germination recovery of annual halophytes have been abundantly documented (Debez et al , Ameixa et al , Shaygan et al ), the regulatory mechanisms at the molecular level during this crucial step of the plant ontogeny remain poorly understood (Tan et al , Kazachkova et al ). Proteomics is a powerful high‐throughput technique to assess the stress‐triggered modulation of large protein datasets at different stages of the plant life cycle.…”

Timing seed germination under changing salinity: a key role of the ERECTA receptor-kinases

“…RGL2 acts as the main GA signalling repressor through activation of a number of transcriptional regulators, including ABI3 and ABI5, the central effectors of ABA signalling, establishment of dormancy, and repression of seed germination (Lopez-Molina et al 2001, 2002; Lee et al, 2002; Piskurewicz et al 2008, 2009; Liu et al 2016). ABI3 and ABI5 are also involved in the regulation of early seedling growth arrest under water stress in Arabidopsis (Lopez-Molina et al 2001; 2002), and in the reversible inhibition of germination in related E.salsugineum under salinity (Kazachkova et al, 2016). To better understand the interaction of the ERf with the ABA regulation of seed germination we monitored the expression of ABI3, ABI5 and RGL2 in WT and er erl1/seg erl2 seeds during germination, and also of DELAY OF GERMINATION1 ( DOG1 ), a pivotal seed dormancy gene which genetically interacts with ABI3 and with a central type 2C protein phosphatase of the ABA signalling pathway during germination, and also regulates ABI5 expression (Dekkers et al 2016; Née et al, 2017; Nishimura et al 2018).…”

Adaptation of Halophytes to Different Habitats

“…These authors suggest that salt inhibits the germination of seeds by inducing a state with molecular characteristics of dormancy, while the layers of the seed coat provide a physical restriction for the emergence of the radicle. This seed status could facilitate survival in saline soils until a rainfall increases the water potential of soil, indicating favorable conditions for seed germination [77]. On the other hand, halophytes adapted to high levels of salinity have useful genes for improving the salinity tolerance of agricultural crops.…”