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Transcriptomic Time-Series Analyses of Gene Expression Profile During Zygotic Embryo Development in Picea mongolica

ABSTRACT: Zygotic embryogenesis is a critical process during seed development in gymnosperms. However, knowledge on the genome-wide transcriptional activation that guides this process in conifers is limited, especially in Picea mongolica. This tree species is endemic to semiarid habitats of Inner Mongolia in China. To extend what is known about the molecular events underpinning its zygotic embryogenesis, comparative transcriptomic analyses of gene expression in zygotic embryos were performed by RNA sequencing in P. mongolica. Our results showed that most changes in transcript levels occurred in the early embryonic pattering determination and formation of mature embryos. Transcripts related to embryogenic competence, cell division pattern, hormones, and stress response genes were identified during embryogenesis. Auxin is essential for early embryo patterning and pre-cotyledon embryonic formation. However, ABA is a major regulator of embryo maturation. Moreover, we found that methylation-related gene expression is associated with activation of early-stage embryos, late embryogenesis abundant proteins, and storage/energy-related genes with late and mature embryos. Furthermore, network analysis revealed stage-specific and multistage gene expression clusters during embryogenesis. WOX, MYB, AP2, and HLH transcription factors seem more relevant to embryogenesis in different stages. Our results provide large-scale and comprehensive transcriptome data for embryo development in P. mongolica. These data will lay a foundation for the protection and utilization of P. mongolica resources.

SUBMITTER: Yan J

PROVIDER: S-EPMC8513737 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: It is during embryogenesis that the plant body plan is established and the meristems responsible for all post-embryonic growth are specified. The molecular mechanisms governing conifer embryogenesis are still largely unknown. Their elucidation may contribute valuable information to clarify if the distinct features of embryo development in angiosperms and gymnosperms result from differential gene regulation. To address this issue, we have performed the first transcriptomic analysis of zygotic embryo development in a conifer species (Pinus pinaster) focusing our study in particular on regulatory genes playing important roles during plant embryo development, namely epigenetic regulators and transcription factors. RESULTS: Microarray analysis of P. pinaster zygotic embryogenesis was performed at five periods of embryo development from early developing to mature embryos. Our results show that most changes in transcript levels occurred in the first and the last embryo stage-to-stage transitions, namely early to pre-cotyledonary embryo and cotyledonary to mature embryo. An analysis of functional categories for genes that were differentially expressed through embryogenesis highlighted several epigenetic regulation mechanisms. While putative orthologs of transcripts associated with mechanisms that target transposable elements and repetitive sequences were strongly expressed in early embryogenesis, PRC2-mediated repression of genes seemed more relevant during late embryogenesis. On the other hand, functions related to sRNA pathways appeared differentially regulated across all stages of embryo development with a prevalence of miRNA functions in mid to late embryogenesis. Identification of putative transcription factor genes differentially regulated between consecutive embryo stages was strongly suggestive of the relevance of auxin responses and regulation of auxin carriers during early embryogenesis. Such responses could be involved in establishing embryo patterning. Later in development, transcripts with homology to genes acting on modulation of auxin flow and determination of adaxial-abaxial polarity were up-regulated, as were putative orthologs of genes required for meristem formation and function as well as establishment of organ boundaries. Comparative analysis with A. thaliana embryogenesis also highlighted genes involved in auxin-mediated responses, as well as epigenetic regulation, indicating highly correlated transcript profiles between the two species. CONCLUSIONS: This is the first report of a time-course transcriptomic analysis of zygotic embryogenesis in a conifer. Taken together our results show that epigenetic regulation and transcriptional control related to auxin transport and response are critical during early to mid stages of pine embryogenesis and that important events during embryogenesis seem to be coordinated by putative orthologs of major developmental regulators in angiosperms.

Project description:BackgroundDespite its relevance, almost no studies account for the genetic control in the early stages of tree development, i.e. from germination on. This study seeks to make a quite complete transcriptome for olive development and to elucidate the dynamic regulation of the transcriptomic response during the early-juvenile period by RNAseq time-series expression analysis. The transcriptome was made from 342,049,597 paired-end reads of 101 bp in length. The assembled transcriptome contained 109,125 unigenes (N50 = 1490 bp, average length = 839).ResultsThe time-series-expression analysis showed that, embryonic structures present at the first month after the induction of germination reached a more differentiated state in two-month-old seedlings. Once the plants were between three and four months old and reached a size around 6-7 nodes, the first developmental stages appeared to be complete and the developing seedling became a juvenile plant. In addition, an AGL-gene was rapidly downregulated during the induction of germination. The repression of this gene was very strong, as evidenced by the low levels of gene expression during plant development from the embryonic seedling to undetectable levels of expression in the adult tree. These results suggest that this gene may be involved in seed dormancy and could be a repressor of the germination. Also, an APL1-like olive gene was found to be expressed at high levels during flowering, and was also expressed during the cold incubation in the activation of embryo germination, suggesting a probable role in embryonic development.ConclusionsThe early development from germination to the juvenile stage of olive seedlings occurred when plants reached a size around 6-7 nodes, and general changes of relevant groups of genes involved in development are described. An AGL-gene was proposed to be involved in germination repression. An APL1-like gene was found to have a probable role in embryonic development.

Project description:Quercus mongolica, a common tree species for building and landscaping in northern China, has great commercial and ecological value. The seedlings of Q. mongolica grow poorly and develop chlorosis when introduced from high-altitude mountains to low-altitude plains. Effective cultivation measures are key to improving the quality of seedlings. To investigate the complex responses of Q. mongolica to different cultivation measures, we compared the adaptability of 3-year-old Q. mongolica seedlings to pruning (P), irrigation (W), and fertilization [F (nitro compound fertilizer with 16N-16P-16K)]. Physiological measurements and transcriptome sequencing were performed on leaves collected under the P treatments (control, cutting, removal of all lateral branches, and removal of base branches to one-third of seedling height), the W treatments (0, 1, 2, 3, 4, or 5 times in sequence), and the F treatments (0, 2, 4, and 6 g/plant). Analyses of the physiological data showed that P was more effective than W or F for activating intracellular antioxidant systems. By contrast, W and F were more beneficial than P for inducing the accumulation of soluble sugar. OPLS-DA identified superoxide dismutase, malondialdehyde, and peroxidase as critical physiological indices for the three cultivation measures. Transcriptome analyses revealed 1,012 differentially expressed genes (DEGs) in the P treatment, 1,035 DEGs in the W treatment, and 1,175 DEGs in the F treatment; these DEGs were mainly enriched in Gene Ontology terms related to the stress response and signal transduction. Weighted gene coexpression network analyses indicated that specific gene modules were significantly correlated with MDA (one module) and soluble sugar (four modules). Functional annotation of the hub genes differentially expressed in MDA and soluble sugar-related modules revealed that Q. mongolica responded and adapted to different cultivation measures by altering signal transduction, hormone levels, reactive oxygen species, metabolism, and transcription factors. The hub genes HOP3, CIPK11, WRKY22, and BHLH35 in the coexpression networks may played a central role in responses to the cultivation practices. These results reveal the mechanism behind the response of Q. mongolica to different cultivation measures at the physiological and molecular levels and provide insight into the response of plants to cultivation measures.

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Transcriptomic Time-Series Analyses of Gene Expression Profile During Zygotic Embryo Development in Picea mongolica

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