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Xylella fastidiosa causes transcriptional shifts that precede tylose formation and starch depletion in xylem

ABSTRACT: Pierce's disease (PD) in grapevine (Vitis vinifera) is caused by the bacterial pathogen Xylella fastidiosa. X. fastidiosa is limited to the xylem tissue and following infection induces extensive plant‐derived xylem blockages, primarily in the form of tyloses. Tylose‐mediated vessel occlusions are a hallmark of PD, particularly in susceptible V. vinifera. We temporally monitored tylose development over the course of the disease to link symptom severity to the level of tylose occlusion and the presence/absence of the bacterial pathogen at fine‐scale resolution. The majority of vessels containing tyloses were devoid of bacterial cells, indicating that direct, localized perception of X. fastidiosa was not a primary cause of tylose formation. In addition, we used X‐ray computed microtomography and machine‐learning to determine that X. fastidiosa induces significant starch depletion in xylem ray parenchyma cells. This suggests that a signalling mechanism emanating from the vessels colonized by bacteria enables a systemic response to X. fastidiosa infection. To understand the transcriptional changes underlying these phenotypes, we integrated global transcriptomics into the phenotypes we tracked over the disease spectrum. Differential gene expression analysis revealed that considerable transcriptomic reprogramming occurred during early PD before symptom appearance. Specifically, we determined that many genes associated with tylose formation (ethylene signalling and cell wall biogenesis) and drought stress were up‐regulated during both Phase I and Phase II of PD. On the contrary, several genes related to photosynthesis and carbon fixation were down‐regulated during both phases. These responses correlate with significant starch depletion observed in ray cells and tylose synthesis in vessels.

ORGANISM(S): Vitis vinifera

PROVIDER: GSE152164 | GEO | 2021/01/19

REPOSITORIES: GEO

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Project description:Wood, or secondary xylem, is the product of xylogenesis, a developmental process that begins with the proliferation of cambial derivatives and ends with mature xylem fibers and vessels with lignified secondary cell walls. Fully mature xylem has undergone a series of cellular processes, including cell division, cell expansion, secondary wall formation, lignification and programmed cell death. A complex network of interactions between transcriptional regulators and signal transduction pathways controls wood formation. However, the role of metabolites during this developmental process has not been comprehensively characterized. To evaluate the role of metabolites during wood formation, we performed a high spatial resolution metabolomics study of the wood-forming zone of Populus tremula, including laser dissected aspen ray and fiber cells. We show that metabolites show specific patterns within the wood-forming zone, following the differentiation process from cell division to cell death. The data from profiled laser dissected aspen ray and fiber cells suggests that these two cell types host distinctly different metabolic processes. Furthermore, by integrating previously published transcriptomic and proteomic profiles generated from the same trees, we provide an integrative picture of molecular processes, for example, deamination of phenylalanine during lignification is of critical importance for nitrogen metabolism during wood formation. UPLC-MS assay of Wood ring and extraxylary tissue is reported in the current study MTBLS1797.GC-MS assay of Wood ring and extraxylary tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1796' rel='noopener noreferrer' target='_blank'>MTBLS1796</a>.UPLC-MS assay of Wood fibre and ray cell tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1831' rel='noopener noreferrer' target='_blank'>MTBLS1831</a>.

Project description:Wood, or secondary xylem, is the product of xylogenesis, a developmental process that begins with the proliferation of cambial derivatives and ends with mature xylem fibers and vessels with lignified secondary cell walls. Fully mature xylem has undergone a series of cellular processes, including cell division, cell expansion, secondary wall formation, lignification and programmed cell death. A complex network of interactions between transcriptional regulators and signal transduction pathways controls wood formation. However, the role of metabolites during this developmental process has not been comprehensively characterized. To evaluate the role of metabolites during wood formation, we performed a high spatial resolution metabolomics study of the wood-forming zone of Populus tremula, including laser dissected aspen ray and fiber cells. We show that metabolites show specific patterns within the wood-forming zone, following the differentiation process from cell division to cell death. The data from profiled laser dissected aspen ray and fiber cells suggests that these two cell types host distinctly different metabolic processes. Furthermore, by integrating previously published transcriptomic and proteomic profiles generated from the same trees, we provide an integrative picture of molecular processes, for example, deamination of phenylalanine during lignification is of critical importance for nitrogen metabolism during wood formation. UPLC-MS assay of Wood fibre and ray cell tissue is reported in the current study MTBLS1831.UPLC-MS assay of Wood ring and extraxylary tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1797' rel='noopener noreferrer' target='_blank'>MTBLS1797</a>.GC-MS assay of Wood ring and extraxylary tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1796' rel='noopener noreferrer' target='_blank'>MTBLS1796</a>.

Project description:Wood, or secondary xylem, is the product of xylogenesis, a developmental process that begins with the proliferation of cambial derivatives and ends with mature xylem fibers and vessels with lignified secondary cell walls. Fully mature xylem has undergone a series of cellular processes, including cell division, cell expansion, secondary wall formation, lignification and programmed cell death. A complex network of interactions between transcriptional regulators and signal transduction pathways controls wood formation. However, the role of metabolites during this developmental process has not been comprehensively characterized. To evaluate the role of metabolites during wood formation, we performed a high spatial resolution metabolomics study of the wood-forming zone of Populus tremula, including laser dissected aspen ray and fiber cells. We show that metabolites show specific patterns within the wood-forming zone, following the differentiation process from cell division to cell death. The data from profiled laser dissected aspen ray and fiber cells suggests that these two cell types host distinctly different metabolic processes. Furthermore, by integrating previously published transcriptomic and proteomic profiles generated from the same trees, we provide an integrative picture of molecular processes, for example, deamination of phenylalanine during lignification is of critical importance for nitrogen metabolism during wood formation. GC-MS assay of Wood ring and extraxylary tissue is reported in the current study MTBLS1796.UPLC-MS assay of Wood ring and extraxylary tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1797' rel='noopener noreferrer' target='_blank'>MTBLS1797</a>.UPLC-MS assay of Wood fibre and ray cell tissue is reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS1831' rel='noopener noreferrer' target='_blank'>MTBLS1831</a>.

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Xylella fastidiosa causes transcriptional shifts that precede tylose formation and starch depletion in xylem

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