Cross-species approaches to seed dormancy and germination: conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes

Abstract

Seed dormancy is genetically determined with substantial environmental influence mediated, at least in part, by the plant hormone abscisic acid (ABA). The ABA-related transcription factor ABI3/VP1 (ABA INSENSITIVE3/VIVIPAROUS1) is widespread among green plants. Alternative splicing of its transcripts appears to be involved in regulating seed dormancy, but the role of ABI3/VP1 goes beyond seeds and dormancy. In contrast, DOG1 (DELAY OF GERMINATION 1), a major quantitative trait gene more specifically involved in seed dormancy, was so far only known from Arabidopsis thaliana (AtDOG1) and whether it also has roles during the germination of non-dormant seeds was not known. Seed germination of Lepidium sativum ('garden cress') is controlled by ABA and its antagonists gibberellins and ethylene and involves the production of apoplastic hydroxyl radicals. We found orthologs of AtDOG1 in the Brassicaceae relatives L. sativum (LesaDOG1) and Brassica rapa (BrDOG1) and compared their gene structure and the sequences of their transcripts expressed in seeds. Tissue-specific analysis of LesaDOG1 transcript levels in L. sativum seeds showed that they are degraded upon imbibition in the radicle and the micropylar endosperm. ABA inhibits germination in that it delays radicle protrusion and endosperm weakening and it increased LesaDOG1 transcript levels during early germination due to enhanced transcription and/or inhibited degradation. A reduced decrease in LesaDOG1 transcript levels upon ABA treatment is evident in the late germination phase in both tissues. This temporal and ABA-related transcript expression pattern suggests a role for LesaDOG1 in the control of germination timing of non-dormant L. sativum seeds. The possible involvement of the ABA-related transcription factors ABI3 and ABI5 in the regulation of DOG1 transcript expression is discussed. Other species of the monophyletic genus Lepidium showed coat or embryo dormancy and are therefore highly suited for comparative seed biology.

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

“…Seed dormancy is induced during seed maturation, and it has been shown in Arabidopsis that seed-specific DOG1 transcript expression starts during seed development 9 d after pollination (DAP) and reaches its highest level during seed maturation. Furthermore, AtDOG1 as well as LesaDOG1 transcripts are present in dry seeds of Arabidopsis and L. sativum, respectively, and transcript levels decline rapidly upon seed imbibition in both species (Bentsink et al, 2006;Graeber et al, 2010). The temporal, spatial, and hormonal LesaDOG1 transcript expression patterns suggest a role of this gene in the control of germination timing of nondormant L. sativum seeds (Graeber et al, 2010).…”

“…Homologs of the AtDOG1 gene are also known for the Brassicaceae species B. rapa (BrDOG1) and Lepidium sativum (Lesa-DOG1; Graeber et al, 2010). However, in contrast to the situation for flowering time and the FLC gene, neither the natural genetic variation at the DOG1 loci of these Arabidopsis relatives nor the distribution of the DOG1 gene in diploid and polyploid Brassicaceae relatives have been investigated.…”

“…However, in contrast to the situation for flowering time and the FLC gene, neither the natural genetic variation at the DOG1 loci of these Arabidopsis relatives nor the distribution of the DOG1 gene in diploid and polyploid Brassicaceae relatives have been investigated. The work of Graeber et al (2010) indicated that LesaDOG1 has functions beyond dormancy (i.e. during the germination of nondormant seeds).…”

“…Furthermore, AtDOG1 as well as LesaDOG1 transcripts are present in dry seeds of Arabidopsis and L. sativum, respectively, and transcript levels decline rapidly upon seed imbibition in both species (Bentsink et al, 2006;Graeber et al, 2010). The temporal, spatial, and hormonal LesaDOG1 transcript expression patterns suggest a role of this gene in the control of germination timing of nondormant L. sativum seeds (Graeber et al, 2010). Recent work shows that the AtDOG1 protein accumulates during seed maturation and, unlike the transcript, remains stable throughout imbibition of Arabidopsis seeds .…”

“…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.…”