Seed maturation in Arabidopsis thaliana is characterized by nuclear size reduction and increased chromatin condensation

Abstract

Most plant species rely on seeds for their dispersal and survival under unfavorable environmental conditions. Seeds are characterized by their low moisture content and significantly reduced metabolic activities. During the maturation phase, seeds accumulate storage reserves and become desiccation-tolerant and dormant. Growth is resumed after release of dormancy and the occurrence of favorable environmental conditions. Here we show that embryonic cotyledon nuclei of Arabidopsis thaliana seeds have a significantly reduced nuclear size, which is established at the beginning of seed maturation. In addition, the chromatin of embryonic cotyledon nuclei from mature seeds is highly condensed. Nuclei regain their size and chromatin condensation level during germination. The reduction in nuclear size is controlled by the seed maturation regulator ABSCISIC ACID-INSENSITIVE 3, and the increase during germination requires two predicted nuclear matrix proteins, LITTLE NUCLEI 1 and LITTLE NUCLEI 2. Our results suggest that the specific properties of nuclei in ripe seeds are an adaptation to desiccation, independent of dormancy. We conclude that the changes in nuclear size and chromatin condensation in seeds are independent, developmentally controlled processes.seed development | seed imbibition | seed germination | chromatin organization P lant seeds represent a quiescent dehydrated state with significantly reduced metabolic activities, which renders them resistant to abiotic stresses and viable for years. Germination occurs when nondormant seeds meet permissive environmental conditions for humidity, light, and temperature. Seed dormancy evolved to postpone germination during unfavorable seasons (1-3). The moisture content of ripe seeds from the model plant Arabidopsis thaliana is <10% (4). Low humidity levels can cause cellular damage due to protein unfolding and membrane disturbance. Sugars, late embryogenesis abundant proteins, and heat shock proteins play important roles in preventing this damage in seeds (5).Dehydration, accumulation of storage reserves, and induction of dormancy occur during the seed maturation phase, which is initiated after the embryo has fully developed (4). In Arabidopsis, seed maturation is tightly controlled by at least four central regulators, ABSCISIC ACID-INSENSITIVE 3 (ABI3), LEAFY COTYLEDON 1 (LEC1), LEC2, and FUSCA 3 (FUS3) (3, 6, 7). Other proteins have more dedicated roles in one of these processes; for instance, DELAY OF GERMINATION 1 (DOG1) and HISTONE MONOUBIQUITINATION 1 (HUB1) are required only for the establishment of seed dormancy (8, 9).Dry seeds represent a transitional state between embryo and seedling. During a phase transition, genes that control the "new" state need to be activated, whereas genes required for the "old" state must be repressed. Chromatin compaction in the cell nucleus has been proposed to contribute to gene regulation by allowing differential accessibility of DNA for the transcription machinery (10, 11). Accordingly, developmental changes in the plant are often ...

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

“…2 and 7). Premature germination can be induced by GAs during Arabidopsis seed development when embryo development has been completed (at approximately 10 DAP), and subsequent seed maturation (approximately 10-20 DAP) includes the induction of primary dormancy (Ooms et al, 1993;Raz et al, 2001;Le et al, 2010;van Zanten et al, 2011). In contrast to Arabidopsis, premature seed germination prior to dormancy induction does not require any hormonal addition in L. papillosum (this work), as is also known from Brassica spp.…”

A Duplicated NUCLEOLIN Gene with Antagonistic Activity Is Required for Chromatin Organization of Silent 45S rDNA in Arabidopsis

“…How do NUC1 and NUC2 functionally interact in Arabidopsis? NUC2 protein accumulation during seedling development (Figure 2) temporally correlates with NOR condensation and rDNA VAR1 repression (Earley et al, 2010;van Zanten et al, 2011;Benoit et al, 2013). Accordingly, upon heterochromatin establishment of NOR2, the expression of NUC2 could be repressed by NUC1 (Figure 3).…”

The LINC complex contributes to heterochromatin organisation and transcriptional gene silencing in plants

“…ATXR5 and ATXR6 are histone H3K27 mono-methyltransferases and the atxr5 atxr6 double mutant displays decondensed chromocentres (Jacob et al, 2009). CRWNs are postulated to be components of the plant lamina-like structure and the crwn1 crwn2 double mutant has previously been described to induce small nuclei (Dittmer et al, 2007) and a more condensed chromatin organisation (Grob et al, 2014;van Zanten et al, 2011;Wang et al, 2013). The quintuple wifi mutant (Zhou and Meier, 2014), lacking three KASH proteins WIP1-WIP3 and the two WPP domaininteracting tail-anchored proteins WIT1 and WIT2, was selected to affect the KASH components of the LINC complex as well as some of its interactors located at the outer nuclear membrane.…”

“…Furthermore, possible candidates for lamin-like and lamin-binding proteins have been identified and are known, respectively, as CROWDED NUCLEI (CRWN) (Dittmer et al, 2007;Wang et al, 2013) and KAKU4 (Goto et al, 2014). Strikingly, sun, wip, kaku4 and crwn mutants all display nuclear shape and/or nuclear size modifications suggesting that mechanical constraints such as those applied by the cytoskeleton at the NE may be released in mutant backgrounds (Dittmer et al, 2007;Goto et al, 2014;Oda and Fukuda, 2011;van Zanten et al, 2011;Zhou et al, 2012). Finally, the SUN-WIP-WIT2-myosin-XI-i complex and CRWN1 have been proposed to independently determine elongated nuclear shape, highlighting the function of cytoskeleton and nucleoskeleton in nuclear morphology (Zhou et al, 2015b).…”

“…Plants are amenable models to study nuclear organisation as natural variations in nuclear morphology occur in various tissues such as epidermis, trichomes and root hairs (Qian et al, 2009;Traas et al, 1998) or during seed formation and germination (van Zanten et al, 2011), as well as in mutants in which the NE or lamin-like components are altered (Dittmer et al, 2007;Goto et al, 2014;Janski et al, 2012;Tamura and Hara-Nishimura, 2011;Zhou et al, 2012). Plants encode a LINC complex consisting of SUN (Sad1 and Unc-84 homology) Graumann et al, 2014) and KASH (Klarsicht, Anc-1 and Syne homology) proteins including WPP domain-interacting proteins (WIPs), SUNinteracting nuclear envelope (SINEs) and TIK (Zhou et al, 2012(Zhou et al, , 2015aGraumann et al, 2014).…”