Transcription Through The Eye Of A Needle: Daily And Annual Cycles Of Gene Expression Variation In Douglas-Fir Needles

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Dolan, Peter ; Cronn, Richard ; Denver, Dee ; Clair, J. ; Neale, David ; Wegrzyn, Jill ; Jogdeo, Sanjuro (2017)
  • Related identifiers: doi: 10.1101/117374
  • Subject: bepress|Life Sciences|Biology | bepress|Life Sciences|Plant Sciences|Plant Biology

Background: Perennial growth in plants is the product of interdependent cycles of daily and annual stimuli that induce cycles of growth and dormancy. In conifers, needles are the key perennial organ that integrates daily and seasonal signals from light, temperature, and water availability. To understand the relationship between seasonal rhythms and seasonal gene expression responses in conifers, we examined diurnal and circannual needle mRNA accumulation in Douglas-fir (Pseudotsuga menziesii) needles at diurnal and circannual scales. Using mRNA sequencing, we sampled 6.1x109 microreads from 19 trees and constructed a de novo pan-transcriptome reference that includes 173,882 tree-derived transcripts. Using this reference, we mapped RNA-Seq reads from 179 samples that capture daily, seasonal, and annual variation. Results: We identified 12,042 diurnally-cyclic transcripts, 9,299 of which showed homology to annotated genes from other plant genomes, including angiosperm core clock genes. Annual analysis revealed 21,225 annually-cyclic transcripts, 17,335 of which showed homology to annotated genes from other plant genomes. The timing of maximum gene expression is associated with light quality at diurnal and photoperiod at annual scales, with two-thirds of transcripts reaching maximum expression +/- 2 hours from sunrise and sunset, and half reaching maximum expression +/- 20 days from winter and summer solstices. Comparison to published microarray-based gene expression studies in spruce (Picea) show that the rank order of expression for 760 putatively orthologous genes was significantly preserved, highlighting the generality of our findings. Conclusions: This finding highlights the extensive annual and seasonal transcriptome variability demonstrated in conifer needles. At these temporal scales, 29% of expressed transcripts showed a significant diurnal rhythm, and 58.7% showed a significant circannual rhythm. Remarkably, thousands of genes reach their annual peak activity during winter dormancy, a time of metabolic stasis. Photoperiod appears to be a dominant driver of annual transcription patterns in Douglas-fir, and these results may be general for predicting rhythmic transcription patterns in emerging gymnosperm models.
  • References (67)
    67 references, page 1 of 7

    1. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, Thomas TL, et al. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 2005;6:544-56.

    2. Dodd AN. Plant circadian clocks increase photosynthesis, growth, survival, and competive advantage. Science. 2005;309:630-3.

    3. McClung CR. Plant circadian rhythms. Plant Cell. 2006;18:792 -803.

    4. Pruneda-Paz JL, Kay SA. An expanding universe of circadian networks in higher plants. Trends Plant Sci. 2010;15:259-65.

    5. Hughes ME, Grant GR, Paquin C, Qian J, Nitabach MN. Deep sequencing the circadian and diurnal transcriptome of Drosophila brain. Genome Res. 2012;22:1266-81.

    6. Dopico XC, Evangelou M, Ferreira RC, Guo H, Pekalski ML, Smyth DJ, et al. Widespread seasonal gene expression reveals annual diefrences in human immunity and physiology. Nat. Commun. 2015;6:7000.

    7. Filichkin SA, Breton G, Priest HD, Dharmawardhana P, Jaiswal P, Fox SE, et al. Global profiling of rice and poplar transcriptomes highlights key conserved circadian-controlled pathways and cis-regulatory modules. PLoS ONE. 2011;6:e16907.

    8. Nagel DH, Doherty CJ, Pruneda-Paz JL, Schmitz RJ, Ecker JR, Kay SA. Genome-wide identifcation of CCA1 targets uncovers an expanded clock network in Arabidopsis. Proc. Natl. Acad. Sci. 2015;112:E4802-E4810.

    9. Ingvarsson PK, García MV, Hall D, Luquez V, Jansson S. Clinal variation in phyB2, a candidate gene for day -length-induced growth cessation and bud set, across a latitudinal gradient in European Aspen (Populus tremula). Genetics. 2006;172:1845- 53.

    10. Horvath DP, Anderson JV, Chao WS, Foley ME. Knowing when to grow: signals regulating bud dormancy. Trends Plant Sci. 2003;8:534-40.

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