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Brief Bioinform , IF:8.99 , 2021 May , V22 (3) doi: 10.1093/bib/bbaa166

A powerful framework for an integrative study with heterogeneous omics data: from univariate statistics to multi-block analysis.

Durufle, Harold and Selmani, Merwann and Ranocha, Philippe and Jamet, Elisabeth and Dunand, Christophe and Dejean, Sebastien

INRAE.; Laboratoire de Recherche en Sciences Vegetales and the Institut de Mathematiques de Toulouse.; CNRS, France.; CNRS and studies plant cell walls.; Toulouse University III-Paul Sabatier.; Institut de Mathematiques, Toulouse University.

High-throughput data generated by new biotechnologies require specific and adapted statistical treatment in order to be efficiently used in biological studies. In this article, we propose a powerful framework to manage and analyse multi-omics heterogeneous data to carry out an integrative analysis. We have illustrated this using the mixOmics package for R software as it specifically addresses data integration issues. Our work also aims at applying the most recent functionalities of mixOmics to real datasets. Although multi-block integrative methodologies exist, we hope to encourage a more widespread use of such approaches in an operational framework by biologists. We have used natural populations of the model plant Arabidopsis thaliana in this work, but the framework proposed is not limited to this plant and can be deployed whatever the organisms of interest and the biological question may be. Four omics datasets (phenomics, metabolomics, cell wall proteomics and transcriptomics) were collected, analysed and integrated to study the cell wall plasticity of plants exposed to sub-optimal temperature growth conditions. The methodologies presented here start from basic univariate statistics leading to multi-block integration analysis. We have also highlighted the fact that each method, either unsupervised or supervised, is associated with one biological issue. Using this powerful framework enabled us to arrive at novel conclusions on the biological system, which would not have been possible using standard statistical approaches.

PMID: 32778869


Plant J , IF:6.141 , 2021 May , V106 (4) : P1163-1176 doi: 10.1111/tpj.15229

Complexity untwined: The structure and function of cucumber (Cucumis sativus L.) shoot phloem.

Sui, Xiaolei and Nie, Jing and Liu, Huan and Lin, Tao and Yao, Xuehui and Turgeon, Robert

Beijing Key Laboratory of Growth and Developmental Regulation for Protected Vegetable Crops, College of Horticulture, China Agricultural University, Beijing, 100193, China.; Plant Biology Section, School of Integrative Plant Science, Cornell University, Ithaca, NY, 14853, USA.

Cucurbit phloem is complex, with large sieve tubes on both sides of the xylem (bicollateral phloem), and extrafascicular elements that form an intricate web linking the rest of the vasculature. Little is known of the physical interconnections between these networks or their functional specialization, largely because the extrafascicular phloem strands branch and turn at irregular angles. Here, export in the phloem from specific regions of the lamina of cucumber (Cucumis sativus L.) was mapped using carboxyfluorescein and (14) C as mobile tracers. We also mapped vascular architecture by conventional microscopy and X-ray computed tomography using optimized whole-tissue staining procedures. Differential gene expression in the internal (IP) and external phloem (EP) was analyzed by laser-capture microdissection followed by RNA-sequencing. The vascular bundles of the lamina form a nexus at the petiole junction, emerging in a predictable pattern, each bundle conducting photoassimilate from a specific region of the blade. The vascular bundles of the stem interconnect at the node, facilitating lateral transport around the stem. Elements of the extrafascicular phloem traverse the stem and petiole obliquely, joining the IP and EP of adjacent bundles. Using pairwise comparisons and weighted gene coexpression network analysis, we found differences in gene expression patterns between the petiole and stem and between IP and EP, and we identified hub genes of tissue-specific modules. Genes related to transport were expressed primarily in the EP while those involved in cell differentiation and development as well as amino acid transport and metabolism were expressed mainly in the IP.

PMID: 33713355


J Exp Bot , IF:5.908 , 2021 May , V72 (12) : P4502-4519 doi: 10.1093/jxb/erab120

Synonymous mutation in Growth Regulating Factor 15 of miR396a target sites enhances photosynthetic efficiency and heat tolerance in poplar.

Zhao, Yiyang and Xie, Jianbo and Wang, Sha and Xu, Weijie and Chen, Sisi and Song, Xueqin and Lu, Mengzhu and El-Kassaby, Yousry A and Zhang, Deqiang

Beijing Advanced Innovation Center for Tree Breeding by Molecular Design, Beijing Forestry University, No. 35, Qinghua East Road, Beijing 100083, P. R. China.; National Engineering Laboratory for Tree Breeding, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China.; Key Laboratory of Genetics and Breeding in Forest Trees and Ornamental Plants, Ministry of Education, College of Biological Sciences and Technology, Beijing Forestry University, Beijing 100083, China.; State Key Laboratory of Tree Genetics and Breeding, Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, China.; Zhejiang Agriculture & Forestry University, Hangzhou 311300, China.; Department of Forest and Conservation Sciences, Faculty of Forestry, Forest Sciences Centre, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.

Heat stress damages plant tissues and induces multiple adaptive responses. Complex and spatiotemporally specific interactions among transcription factors (TFs), microRNAs (miRNAs), and their targets play crucial roles in regulating stress responses. To explore these interactions and to identify regulatory networks in perennial woody plants subjected to heat stress, we integrated time-course RNA-seq, small RNA-seq, degradome sequencing, weighted gene correlation network analysis, and multi-gene association approaches in poplar. Results from Populus trichocarpa enabled us to construct a three-layer, highly interwoven regulatory network involving 15 TFs, 45 miRNAs, and 77 photosynthetic genes. Candidate gene association studies in a population of P. tomentosa identified 114 significant associations and 696 epistatic SNP-SNP pairs that were linked to 29 photosynthetic and growth traits (P<0.0001, q<0.05). We also identified miR396a and its target, Growth-Regulating Factor 15 (GRF15) as an important regulatory module in the heat-stress response. Transgenic plants of hybrid poplar (P. alba x P. glandulosa) overexpressing a GRF15 mRNA lacking the miR396a target sites exhibited enhanced heat tolerance and photosynthetic efficiency compared to wild-type plants. Together, our observations demonstrate that GRF15 plays a crucial role in responding to heat stress, and they highlight the power of this new, multifaceted approach for identifying regulatory nodes in plants.

PMID: 33711151


Ecology , IF:4.7 , 2021 May : Pe03384 doi: 10.1002/ecy.3384

Environmental variation drives continental-scale synchrony of European beech reproduction.

Bogdziewicz, Michal and Hacket-Pain, Andrew and Ascoli, Davide and Szymkowiak, Jakub

Department of Systematic Zoology, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland.; Department of Geography and Planning, School of Environmental Sciences, University of Liverpool, Liverpool, UK.; Department of Agricultural, Forestry and Food Sciences, University of Torino, Grugliasco, Italy.; Population Ecology Research Unit, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland.

Spatial synchrony is the tendency of spatially separated populations to display similar temporal fluctuations. Synchrony affects regional ecosystem functioning, but it remains difficult to disentangle its underlying mechanisms. We leveraged regression on distance matrices and geography of synchrony to understand the processes driving synchrony of European beech masting over the European continent. Masting in beech shows distance-decay, but significant synchrony is maintained at spatial scales of up to 1500 km. The spatial synchrony of the weather cues that drive interannual variation in reproduction also explains the regional spatial synchrony of masting. Proximity played no apparent role in influencing beech masting synchrony after controlling for synchrony in environmental variation. Synchrony of beech reproduction shows a clear biogeographical pattern, decreasing from the northwest to southeast Europe. Synchrony networks for weather cues resemble networks for beech masting, indicating that the geographical structure of weather synchrony underlies the biogeography of masting synchrony. Our results support the hypothesis that environmental factors, the Moran effect, are key drivers of spatial synchrony in beech seed production at regional scales. The geographical patterns of regional synchronization of masting have implications for regional forest production, gene flow, carbon cycling, disease dynamics, biodiversity, and conservation.

PMID: 33950521