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Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death.

ABSTRACT: The terminal differentiation and elimination of the embryo-suspensor is the earliest manifestation of programmed cell death (PCD) during plant ontogenesis. Molecular regulation of suspensor PCD remains poorly understood. Norway spruce (Picea abies) embryos provide a powerful model for studying embryo development because of their large size, sequenced genome, and the possibility to obtain a large number of embryos at a specific developmental stage through somatic embryogenesis. Here, we have carried out global gene expression analysis of the Norway spruce embryo-suspensor versus embryonal mass (a gymnosperm analogue of embryo proper) using RNA sequencing. We have identified that suspensors have enhanced expression of the NAC domain-containing transcription factors, XND1 and ANAC075, previously shown to be involved in the initiation of developmental PCD in Arabidiopsis. The analysis has also revealed enhanced expression of Norway spruce homologues of the known executioners of both developmental and stress-induced cell deaths, such as metacaspase 9 (MC9), cysteine endopeptidase-1 (CEP1) and ribonuclease 3 (RNS3). Interestingly, a spruce homologue of bax inhibitor-1 (PaBI-1, for Picea abies BI-1), an evolutionarily conserved cell death suppressor, was likewise up-regulated in the embryo-suspensor. Since Arabidopsis BI-1 so far has been implicated only in the endoplasmic reticulum (ER)-stress induced cell death, we investigated its role in embryogenesis and suspensor PCD using RNA interference (RNAi). We have found that PaBI-1-deficient lines formed a large number of abnormal embryos with suppressed suspensor elongation and disturbed polarity. Cytochemical staining of suspensor cells has revealed that PaBI-1 deficiency suppresses vacuolar cell death and induces necrotic type of cell death previously shown to compromise embryo development. This study demonstrates that a large number of cell-death components are conserved between angiosperms and gymnosperms and establishes a new role for BI-1 in the progression of vacuolar cell death.

SUBMITTER: Reza SH

PROVIDER: S-EPMC5834160 | biostudies-literature | 2018

REPOSITORIES: biostudies-literature

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Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death.

Reza Salim H SH Delhomme Nicolas N Street Nathaniel R NR Ramachandran Prashanth P Dalman Kerstin K Nilsson Ove O Minina Elena A EA Bozhkov Peter V PV

PloS one 20180302 3

The terminal differentiation and elimination of the embryo-suspensor is the earliest manifestation of programmed cell death (PCD) during plant ontogenesis. Molecular regulation of suspensor PCD remains poorly understood. Norway spruce (Picea abies) embryos provide a powerful model for studying embryo development because of their large size, sequenced genome, and the possibility to obtain a large number of embryos at a specific developmental stage through somatic embryogenesis. Here, we have carr ...[more]

PMID: 29499063

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Project description:Drought stress impacts seedling establishment, survival and whole-plant productivity. Molecular responses to drought stress have been most extensively studied in herbaceous species, mostly considering only aboveground tissues. Coniferous tree species dominate boreal forests, which are predicted to be exposed to more frequent and acute drought as a result of ongoing climate change. The associated impact at all stages of the forest tree life cycle is expected to have large-scale ecological and economic impacts. However, the molecular response to drought has not been comprehensively profiled for coniferous species. We assayed the physiological and transcriptional response of Picea abies (L.) H. Karst seedling needles and roots after exposure to mild and severe drought. Shoots and needles showed an extensive reversible plasticity for physiological measures indicative of drought-response mechanisms, including changes in stomatal conductance (gs), shoot water potential and abscisic acid (ABA). In both tissues, the most commonly observed expression profiles in response to drought were highly correlated with the ABA levels. Still, root and needle transcriptional responses contrasted, with extensive root-specific down-regulation of growth. Comparison between previously characterized Arabidopsis thaliana L. drought-response genes and P. abies revealed both conservation and divergence of transcriptional response to drought. In P. abies, transcription factors belonging to the ABA responsive element(ABRE) binding/ABRE binding factors ABA-dependent pathway had a more limited role. These results highlight the importance of profiling both above- and belowground tissues, and provide a comprehensive framework to advance the understanding of the drought response of P. abies. The results demonstrate that a short-term, severe drought induces severe physiological responses coupled to extensive transcriptome modulation and highlight the susceptibility of Norway spruce seedlings to such drought events.

Project description:The mechanisms by which different light spectra regulate plant shoot elongation vary, and phytohormones respond differently to such spectrum-associated regulatory effects. Light supplementation can effectively control seedling growth in Norway spruce. However, knowledge of the effective spectrum for promoting growth and phytohormone metabolism in this species is lacking. In this study, 3-year-old Norway spruce clones were illuminated for 12 h after sunset under blue or red light-emitting diode (LED) light for 90 d, and stem increments and other growth traits were determined. Endogenous hormone levels and transcriptome differences in the current needles were assessed to identify genes related to the red and blue light regulatory responses. The results showed that the stem increment and gibberellin (GA) levels of the seedlings illuminated by red light were 8.6% and 29.0% higher, respectively, than those of the seedlings illuminated by blue light. The indoleacetic acid (IAA) level of the seedlings illuminated by red light was 54.6% lower than that of the seedlings illuminated by blue light, and there were no significant differences in abscisic acid (ABA) or zeatin riboside [ZR] between the two groups of seedlings. The transcriptome results revealed 58,736,166 and 60,555,192 clean reads for the blue-light- and red-light-illuminated samples, respectively. Illumina sequencing revealed 21,923 unigenes, and 2744 (approximately 93.8%) out of 2926 differentially expressed genes (DEGs) were found to be upregulated under blue light. The main KEGG classifications of the DEGs were metabolic pathway (29%), biosynthesis of secondary metabolites (20.49%) and hormone signal transduction (8.39%). With regard to hormone signal transduction, AUXIN-RESISTANT1 (AUX1), AUX/IAA genes, auxin-inducible genes, and early auxin-responsive genes [(auxin response factor (ARF) and small auxin-up RNA (SAUR)] were all upregulated under blue light compared with red light, which might have yielded the higher IAA level. DELLA and phytochrome-interacting factor 3 (PIF3), involved in negative GA signaling, were also upregulated under blue light, which may be related to the lower GA level. Light quality also affects endogenous hormones by influencing secondary metabolism. Blue light promoted phenylpropanoid biosynthesis, phenylalanine metabolism, flavonoid biosynthesis and flavone and flavonol biosynthesis, accompanied by upregulation of most of the genes in their pathways. In conclusion, red light may promote stem growth by regulating biosynthesis of GAs, and blue light may promote flavonoid, lignin, phenylpropanoid and some hormones (such as jasmonic acid) which were related to plant defense in Norway spruce, which might reduce the primary metabolites available for plant growth.

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Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death.

Publications

Transcriptome analysis of embryonic domains in Norway spruce reveals potential regulators of suspensor cell death.

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