Ethylene Interacts with Abscisic Acid to Regulate Endosperm Rupture during Germination: A Comparative Approach UsingLepidium sativumandArabidopsis thaliana   

Abstract

The micropylar endosperm cap covering the radicle in the mature seeds of most angiosperms acts as a constraint that regulates seed germination. Here, we report on a comparative seed biology study with the close Brassicaceae relatives Lepidium sativum and Arabidopsis thaliana showing that ethylene biosynthesis and signaling regulate seed germination by a mechanism that requires the coordinated action of the radicle and the endosperm cap. The larger seed size of Lepidium allows direct tissue-specific biomechanical, biochemical, and transcriptome analyses. We show that ethylene promotes endosperm cap weakening of Lepidium and endosperm rupture of both species and that it counteracts the inhibitory action of abscisic acid (ABA) on these two processes. Cross-species microarrays of the Lepidium micropylar endosperm cap and the radicle show that the ethylene-ABA antagonism involves both tissues and has the micropylar endosperm cap as a major target. Ethylene counteracts the ABA-induced inhibition without affecting seed ABA levels. The Arabidopsis loss-of-function mutants ACC oxidase2 (aco2; ethylene biosynthesis) and constitutive triple response1 (ethylene signaling) are impaired in the 1-aminocyclopropane-1-carboxylic acid (ACC)-mediated reversion of the ABA-induced inhibition of seed germination. Ethylene production by the ACC oxidase orthologs Lepidium ACO2 and Arabidopsis ACO2 appears to be a key regulatory step. Endosperm cap weakening and rupture are promoted by ethylene and inhibited by ABA to regulate germination in a process conserved across the Brassicaceae.

Spatiotemporal Seed Development Analysis Provides Insight into Primary Dormancy Induction and Evolution of theLepidium DELAY OF GERMINATION1Genes

“…Comparative work with Lepidium spp. and Arabidopsis seeds (Linkies et al, 2009;Graeber et al, 2010Graeber et al, , 2011Voegele et al, 2011), fruits Mühlhausen et al, 2010), and flowers (Lee et al, 2002) emphasizes that the genus Lepidium provides a phylogenetically and environmentally defined framework highly suited for evolutionary and developmental research on seed/ fruit-related traits. DOG1 gene homologs are present in Lepidium spp.…”

“…Each FO contains 16 seeds, of which we used one-half for the germination assays and one-half for protein analyses; however, as each seed is large enough, several further single-seed-based biochemical assays also would be possible. In summary, the genus Lepidium harbors species with scientifically interesting and experimentally advantageous features, such as the nondormant and large-seeded L. sativum that emerged as a Brassicaceae model to study endosperm weakening during seed germination (Linkies et al, 2009;Graeber et al, 2010;Voegele et al, 2012), as well as species with dormant seeds like L. papillosum, for which dormancy induction during seed maturation can be studied with a superior spatiotemporal resolution.…”

“…Intercontinental dispersal of mucilaginous seeds adhering to birds led to a relatively rapid worldwide distribution, forming the basis for adaptations to very different habitats (Mummenhoff et al, 2004;Dierschke et al, 2009). Comparative work with L. sativum and Arabidopsis seeds (Linkies et al, 2009;Graeber et al, 2010Graeber et al, , 2011Voegele et al, 2011) and fruits Mühlhausen et al, 2010) highlights the suitability of the genus Lepidium for cross-species research on diverse developmental aspects. Here, we exploit the experimental advantage of the highly structured Lepidium papillosum infructescence (i.e.…”

Seed-Specific Expression of a Feedback-Insensitive Form of CYSTATHIONINE-γ-SYNTHASE in Arabidopsis Stimulates Metabolic and Transcriptomic Responses Associated with Desiccation Stress

“…One possible explanation can be that the SSE seeds may have higher levels of ET, which was found to play a crucial role in overcoming seed dormancy and can alleviate germination inhibition induced by salinity in many seeds (Lin et al, 2013). Moreover, a negative interaction between ET and ABA, in which ET can overcome the inhibitory action of ABA in seeds, was reported (Linkies et al, 2009). Another possible explanation for the ability of these seeds to germinate better than wild-type seeds under stress is the higher stress-related metabolites such as sugars, BCAAs, polyamines, and different transcripts found in these seeds.…”

The E3 ubiquitin ligase HOS1 is involved in ethylene regulation of leaf expansion inArabidopsis

“…[5][6][7] The simple hydrocarbon ethylene is a gaseous plant hormone that regulates a variety of developmental processes, such as seed germination, cell elongation, abscission, senescence, sex determination, and fruit ripening. [8][9][10][11][12][13] It has been also proposed that ethylene negatively regulates leaf expansion process. Exogenous ethylene treatment results in reduced leaf area.…”