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Physcomitrium patens Infection by Colletotrichum gloeosporioides: Understanding the Fungal-Bryophyte Interaction by Microscopy, Phenomics and RNA Sequencing.

ABSTRACT: Anthracnose caused by the hemibiotroph fungus Colletotrichum gloeosporioides is a devastating plant disease with an extensive impact on plant productivity. The process of colonization and disease progression of C. gloeosporioides has been studied in a number of angiosperm crops. To better understand the evolution of the plant response to pathogens, the study of this complex interaction has been extended to bryophytes. The model moss Physcomitrium patens Hedw. B&S (former Physcomitrella patens) is sensitive to known bacterial and fungal phytopathogens, including C. gloeosporioides, which cause infection and cell death. P. patens responses to these microorganisms resemble that of the angiosperms. However, the molecular events during the interaction of P. patens and C. gloeosporioides have not been explored. In this work, we present a comprehensive approach using microscopy, phenomics and RNA-seq analysis to explore the defense response of P. patens to C. gloeosporioides. Microscopy analysis showed that appressoria are already formed at 24 h after inoculation (hai) and tissue colonization and cell death occur at 24 hai and is massive at 48 hai. Consequently, the phenomics analysis showed progressing browning of moss tissues and impaired photosynthesis from 24 to 48 hai. The transcriptomic analysis revealed that more than 1200 P. patens genes were differentially expressed in response to Colletotrichum infection. The analysis of differentially expressed gene function showed that the C. gloeosporioides infection led to a transcription reprogramming in P. patens that upregulated the genes related to pathogen recognition, secondary metabolism, cell wall reinforcement and regulation of gene expression. In accordance with the observed phenomics results, some photosynthesis and chloroplast-related genes were repressed, indicating that, under attack, P. patens changes its transcription from primary metabolism to defend itself from the pathogen.

SUBMITTER: Otero-Blanca A

PROVIDER: S-EPMC8401727 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The limit of the Colletotrichum gloeosporioides species complex is defined genetically, based on a strongly supported clade within the Colletotrichum ITS gene tree. All taxa accepted within this clade are morphologically more or less typical of the broadly defined C. gloeosporioides, as it has been applied in the literature for the past 50 years. We accept 22 species plus one subspecies within the C. gloeosporioides complex. These include C. asianum, C. cordylinicola, C. fructicola, C. gloeosporioides, C. horii, C. kahawae subsp. kahawae, C. musae, C. nupharicola, C. psidii, C. siamense, C. theobromicola, C. tropicale, and C. xanthorrhoeae, along with the taxa described here as new, C. aenigma, C. aeschynomenes, C. alatae, C. alienum, C. aotearoa, C. clidemiae, C. kahawae subsp. ciggaro, C. salsolae, and C. ti, plus the nom. nov. C. queenslandicum (for C. gloeosporioides var. minus). All of the taxa are defined genetically on the basis of multi-gene phylogenies. Brief morphological descriptions are provided for species where no modern description is available. Many of the species are unable to be reliably distinguished using ITS, the official barcoding gene for fungi. Particularly problematic are a set of species genetically close to C. musae and another set of species genetically close to C. kahawae, referred to here as the Musae clade and the Kahawae clade, respectively. Each clade contains several species that are phylogenetically well supported in multi-gene analyses, but within the clades branch lengths are short because of the small number of phylogenetically informative characters, and in a few cases individual gene trees are incongruent. Some single genes or combinations of genes, such as glyceraldehyde-3-phosphate dehydrogenase and glutamine synthetase, can be used to reliably distinguish most taxa and will need to be developed as secondary barcodes for species level identification, which is important because many of these fungi are of biosecurity significance. In addition to the accepted species, notes are provided for names where a possible close relationship with C. gloeosporioides sensu lato has been suggested in the recent literature, along with all subspecific taxa and formae speciales within C. gloeosporioides and its putative teleomorph Glomerella cingulata.Taxonomic noveltiesName replacement - C. queenslandicum B. Weir & P.R. Johnst. New species - C. aenigma B. Weir & P.R. Johnst., C. aeschynomenes B. Weir & P.R. Johnst., C. alatae B. Weir & P.R. Johnst., C. alienum B. Weir & P.R. Johnst, C. aotearoa B. Weir & P.R. Johnst., C. clidemiae B. Weir & P.R. Johnst., C. salsolae B. Weir & P.R. Johnst., C. ti B. Weir & P.R. Johnst. New subspecies - C. kahawae subsp. ciggaro B. Weir & P.R. Johnst. Typification: Epitypification - C. queenslandicum B. Weir & P.R. Johnst.

Project description:Mosses are an ancient land plant lineage and are therefore important in studying the evolution of plant developmental processes. Here, we describe stomatal development in the model moss species Physcomitrium patens (previously known as Physcomitrella patens) over the duration of sporophyte development. We dissect the molecular mechanisms guiding cell division and fate and highlight how stomatal function might vary under different environmental conditions. In contrast to the asymmetric entry divisions described in Arabidopsis thaliana, moss protodermal cells can enter the stomatal lineage directly by expanding into an oval shaped guard mother cell (GMC). We observed that when two early stage P. patens GMCs form adjacently, a spacing division can occur, leading to separation of the GMCs by an intervening epidermal spacer cell. We investigated whether orthologs of Arabidopsis stomatal development regulators are required for this spacing division. Our results indicated that bHLH transcription factors PpSMF1 and PpSCRM1 are required for GMC formation. Moreover, the ligand and receptor components PpEPF1 and PpTMM are also required for orientating cell divisions and preventing single or clustered early GMCs from developing adjacent to one another. The identification of GMC spacing divisions in P. patens raises the possibility that the ability to space stomatal lineage cells could have evolved before mosses diverged from the ancestral lineage. This would have enabled plants to integrate stomatal development with sporophyte growth and could underpin the adoption of multiple bHLH transcription factors and EPF ligands to more precisely control stomatal patterning in later diverging plant lineages. We also observed that when P. patens sporophyte capsules mature in wet conditions, stomata are typically plugged whereas under drier conditions this is not the case; instead, mucilage drying leads to hollow sub-stomatal cavities. This appears to aid capsule drying and provides further evidence for early land plant stomata contributing to capsule rupture and spore release.

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Physcomitrium patens Infection by Colletotrichum gloeosporioides: Understanding the Fungal-Bryophyte Interaction by Microscopy, Phenomics and RNA Sequencing.

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