Stress induces plant somatic cells to acquire some features of stem cells accompanied by selective chromatin reorganization

Abstract

Background: Previous data suggested that senescing cells or cells exposed to acute stress may acquire stem cell properties characterized by open chromatin conformation and by promiscuous expression of transcription factor genes. To further explore the link between stress response and dedifferentiation, we generated transgenic plants in which a reporter AtMBD6-GFP is controlled by a meristem-specific promoter derived from the ANAC2 gene together with the analysis of chromatin conformation. Results: We found that ANAC2 promoter is essentially active in the shoot and the root apical meristems including leaf primordia. ANAC2 was activated in mature leaves following exposure to various stress conditions including protoplasting and dark. This activity was associated with decondensation of pericentric but not of centromeric chromatin. Using epigenetic mutants, ddm1 and kyp/suvh4, we found that compaction at centromeric chromatin persists despite a significant reduction in DNA and histone methylation. Conclusions: Our results suggest that extreme environmental signals trigger plant somatic cells to acquire stem cell properties before assuming a new cell fate. Results also pointed to distinct mechanisms involved in controlling chromatin compaction at chromocenter and that compaction of centromeric chromatin may not be dependent on epigenetic means driven by DDM1 and KYP/SUVH4 chromatin modifier proteins. Developmental Dynamics 242:1121-1133, 2013. V C 2013 Wiley Periodicals, Inc.Key words: stress response; dedifferentiation; chromatin reorganization; DNA methylation; histone modifications; Arabidopsis Key Findings:Acute stress induces, in leaf cells, the activity of a meristem-specific promoter derived from the ANAC2 transcription factor-encoding gene. Stressed leaf cells acquire a dedifferentiated state characterized by open chromatin conformation. Stress-induced chromatin decondensation is selective for peri-centromeric but not centromeric region.Maintenance of hetrochromatin at centromeric region is not dependent on DNA and histone methylation driven by DDM1 and KYP/SUVH4 proteins.

Transcriptome analysis indicates that GmAGAMOUS-Like 15 may enhance somatic embryogenesis by promoting a dedifferentiated state

“…14 Stress caused by dark-induced premature senescence that up-regulates ANAC2, also leads to increased callus formation, possibly by dedifferentiation mediated by ANAC2. 14 The second class of transcription factors Grafi et al 13 highlight are members of the WRKY family. WRKY TFs are often involved in stress responses.…”

Advancing Crop Transformation in the Era of Genome Editing

“…The choice of growth regulators and their sequence and timing of exposure are currently determined empirically for each species and often adjusted for each genotype. The molecular mechanisms for induction of cultured tissues from somatic cells are becoming better understood, and stress plays a striking role in this process (Florentin et al, 2013;Ikeuchi et al, 2013;Fehér, 2015;Grafi and Barack, 2015). Genetic and epigenetic mechanisms appear to control callus formation and the redifferentiation of organs and somatic embryos from different tissues through modulating hormonal signaling involving AUXIN RESPONSE FACTORs (Fan et al, 2012); cytokinin type-B ARABIDOPSIS RESPONSE REGULATORs (Sakai et al, 2001;Tajima et al, 2004); transcription factors, such as LEAFY COTYLEDON1 (LEC1), WUSCHEL (WUS), and BABY BOOM (ODP2); AGAMOUS-LIKE15; and the SOMATIC EMBRYOGENESIS RECEPTOR KINASE (reviewed in Ikeuchi et al, 2013;Fehér, 2015).…”

“…The RECEPTOR-LIKE PROTEIN KINASE1, an abscisic acidrelated receptor, appears to be important for the regeneration capacity of calli induced in Arabidopsis roots (Motte et al, 2014). Epigenetic regulation (chromatin remodeling) through DNA methylation and histone modification directly affect the expression of many of the key regulators of cell proliferation and differentiation (Zhao et al, 2001;Furuta et al, 2011;Florentin et al, 2013). Surprisingly, altering endogenous changes in plant developmental biology via genetic manipulation is an underutilized approach.…”

Involvement of Plant Stem Cells or Stem Cell-Like Cells in Dedifferentiation

“…Auxin and cytokinin induce protoplasts to reenter the cell cycle, proliferate, and form callus ( Grafi, 2004 ; Muraro et al, 2011 ). Stress conditions, including protoplasting (plant cell wall is degraded by enzymes), wounding, and exposure to dark or heat, induce somatic cells to change their fate via dedifferentiation ( Malamy, 2005 ; Grafi et al, 2011a , b ; Florentin et al, 2013 ; Feher, 2014 ). Researchers propose that the dedifferentiated state is a transient state of senescence because senescing cells share similar features, such as gene expression and chromatin modification, with dedifferentiating protoplast cells ( Balazadeh et al, 2008 ; Damri et al, 2009 ; Yadav et al, 2009 ).…”