{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,4]],"date-time":"2026-07-04T02:16:21Z","timestamp":1783131381562,"version":"3.54.6"},"reference-count":38,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,7,12]],"date-time":"2022-07-12T00:00:00Z","timestamp":1657584000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Plant Sci."],"abstract":"<jats:p>Downy mildew of foxtail millet is an important oomycete disease caused by <jats:italic>Sclerospora graminicola<\/jats:italic>, affecting the yield and quality of the crop. Foxtail millet infected with <jats:italic>S. graminicola<\/jats:italic> exhibit symptoms of leaf yellowing and leaf cracking. To uncover the pathogenic mechanism of this disease, we explored the effects on chlorophyll synthesis and photosynthesis of foxtail millet leaves infected by <jats:italic>S. graminicola<\/jats:italic>. An elite foxtail millet variety, JG21, susceptible to <jats:italic>S. graminicola<\/jats:italic>, was used as for this study. <jats:italic>S. graminicola<\/jats:italic> inhibited chlorophyll synthesis and caused loose mesophyll cell arrangement. In addition, some cells were severely vacuolated in <jats:italic>S. graminicola<\/jats:italic>-infected foxtail millet leaves at the early stages of infection. <jats:italic>S. graminicola<\/jats:italic> could invade the mesophyll cells through haustoria which destroyed the chloroplast structure at the middle stages of infection causing significant accumulation of osmiophilic particles (OPs) and disintegrated chloroplast grana lamellae. Furthermore, foxtail millet leaves split longitudinally at the later stages of infection. Chlorophyll and carotenoid contents in infected leaves decreased significantly compared with those in the control. Net photosynthetic rate (Pn) of leaves and stomatal conductance showed a downward trend, and intercellular carbon dioxide concentrations increased significantly following the infection with <jats:italic>S. graminicola<\/jats:italic>. A total of 1,618 differentially expressed genes (DEGs) were detected between the control group and the treatment groups using RNA sequencing (RNA-Seq) among S1\u2013S5 stages. DEGs associated with \u201cphotosynthesis\u201d and \u201clight reaction\u201d were enriched. Gene expression patterns showed that 91.3% of 23 genes related to chlorophyll synthesis and photosynthesis, were significantly down-regulated than the control during S1\u2013S5 stages. Based on the gene expression dataset, weighed gene co-expression network analysis (WGCNA) with 19 gene co-expression modules related to photosynthesis revealed six hub genes related to chlorophyll synthesis, which were suppressed during infection. The results suggest that infection of <jats:italic>S. graminicola<\/jats:italic> led to weak chlorophyll synthesis and rapid chloroplasts disappearance in foxtail millet. The defense responses and resistance of foxtail millet to <jats:italic>S. graminicola<\/jats:italic> were inhibited because chloroplast structure and function were destroyed in leaves, and the sexual reproduction in <jats:italic>S. graminicola<\/jats:italic> could be completed rapidly.<\/jats:p>","DOI":"10.3389\/fpls.2022.928040","type":"journal-article","created":{"date-parts":[[2022,7,12]],"date-time":"2022-07-12T13:32:58Z","timestamp":1657632778000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":4,"title":["Sclerospora graminicola Suppresses Plant Defense Responses by Disrupting Chlorophyll Biosynthesis and Photosynthesis in Foxtail Millet"],"prefix":"10.3389","volume":"13","author":[{"given":"Baojun","family":"Zhang","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xu","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yurong","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lin","family":"Xu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhixian","family":"Ren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaofei","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yuanhuai","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,7,12]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1007\/s00425-006-0303-3","article-title":"Infection with virulent and avirulent P. Syringae strains differentially affects photosynthesis and sink metabolism in Arabidopsis leaves.","volume":"225","author":"Bonfig","year":"2006","journal-title":"Planta"},{"key":"B2","doi-asserted-by":"publisher","first-page":"290","DOI":"10.3321\/j.issn:0412-0914.2009.03.011","article-title":"Relationships between canopy reflectance and chlorophyll contents of wheat infected with powdery mildew in fields.","volume":"39","author":"Cao","year":"2009","journal-title":"Acta Phytopathol. Sin."},{"key":"B3","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1016\/j.devcel.2015.05.011","article-title":"Chloroplast stromules function during innate immunity.","volume":"34","author":"Caplan","year":"2015","journal-title":"Dev. Cell."},{"key":"B4","doi-asserted-by":"publisher","first-page":"25","DOI":"10.1146\/annurev-arplant-043015-111854","article-title":"Learning the languages of the chloroplast: retrograde signaling and beyond.","volume":"67","author":"Chan","year":"2016","journal-title":"Annu. Rev. Plant Biol."},{"key":"B5","doi-asserted-by":"publisher","first-page":"1194","DOI":"10.1016\/j.molp.2020.06.009","article-title":"Tbtools: an integrative toolkit developed for interactive analyses of big biological data.","volume":"13","author":"Chen","year":"2020","journal-title":"Mol. Plant."},{"key":"B6","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-10760-6","article-title":"Oxidative post-translational modification of executer1 is required for singlet oxygen sensing in plastids.","volume":"27","author":"Dogra","year":"2019","journal-title":"Nat. Commun."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1399","DOI":"10.1007\/s11274-013-1564-1","article-title":"Fusaric acid accelerates the senescence of leaf in banana when infected by Fusarium.","volume":"30","author":"Dong","year":"2014","journal-title":"World J. Microbiol. Biotechnol."},{"key":"B8","doi-asserted-by":"publisher","first-page":"469","DOI":"10.1094\/PDIS.1997.81.5.469","article-title":"Reduced dosage of methyl bromide for controlling verticillium wilt of potato in experimental and commercial plots.","volume":"81","author":"Gamliel","year":"1997","journal-title":"Plant Dis."},{"key":"B9","doi-asserted-by":"publisher","first-page":"9613","DOI":"10.1073\/pnas.2002759117","article-title":"Pathogen manipulation of chloroplast function triggers a light-dependent immune recognition.","volume":"117","author":"Gao","year":"2020","journal-title":"Proc. Natl. Acad. Sci. U S A."},{"key":"B10","doi-asserted-by":"publisher","DOI":"10.1038\/srep41610","article-title":"Alterations in rice chloroplast integrity, photosynthesis and metabolome associated with pathogenesis of Rhizoctonia Solani.","volume":"7","author":"Ghosh","year":"2017","journal-title":"Sci. Rep."},{"key":"B11","doi-asserted-by":"publisher","first-page":"829","DOI":"10.1094\/MPMI-03-17-0055-R","article-title":"The sal-pap chloroplast retrograde pathway contributes to plant immunity by regulating glucosinolate pathway and phytohormone signaling.","volume":"30","author":"Ishiga","year":"2017","journal-title":"Mol. Plant Microbe Interact."},{"key":"B12","doi-asserted-by":"publisher","first-page":"199","DOI":"10.1016\/j.cub.2007.02.028","article-title":"A J domain virulence effector of Pseudomonas Syringae remodels host chloroplasts and suppresses defenses.","volume":"17","author":"Jelenska","year":"2007","journal-title":"Curr. Biol."},{"key":"B13","doi-asserted-by":"publisher","DOI":"10.3390\/genes10090658","article-title":"Autophagy related gene (Atg3) is a key regulator for cell growth, development, and virulence of fusarium oxysporum.","volume":"10","author":"Khalid","year":"2019","journal-title":"Genes."},{"key":"B14","first-page":"299","author":"Kupeevicz","year":"1947","journal-title":"The Physiology of the Diseased Plant in Relation to the General Questions of Parasitism."},{"key":"B15","doi-asserted-by":"publisher","DOI":"10.1186\/1471-2105-9-559","article-title":"Wgcna: an R package for weighted correlation network analysis.","volume":"9","author":"Langfelder","year":"2008","journal-title":"BMC Bioinformat."},{"key":"B16","doi-asserted-by":"publisher","first-page":"351","DOI":"10.1016\/j.chom.2020.08.006","article-title":"A fight between plants and pathogens for the control of chloroplasts.","volume":"28","author":"Lee","year":"2020","journal-title":"Cell Host Microbe."},{"key":"B17","doi-asserted-by":"publisher","first-page":"310","DOI":"10.1111\/tpj.12396","article-title":"Distinct Pseudomonas type-III effectors use a cleavable transit peptide to target chloroplasts.","volume":"77","author":"Li","year":"2014","journal-title":"Plant J."},{"key":"B18","doi-asserted-by":"publisher","DOI":"10.3390\/ijms21041226","article-title":"Transcriptome profiling analysis reveals co-regulation of hormone pathways in foxtail millet during Sclerospora Graminicola infection.","volume":"21","author":"Li","year":"2020","journal-title":"Int. J. Mol. Sci."},{"key":"B19","doi-asserted-by":"publisher","first-page":"3088","DOI":"10.1111\/nph.17076","article-title":"Chloroplast immunity illuminated.","volume":"229","author":"Littlejohn","year":"2020","journal-title":"New Phytol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"1557","DOI":"10.1111\/tpj.15252","article-title":"A Plasmopara Viticola Rxlr effector targets a chloroplast protein Psbp to inhibit ros production in grapevine.","volume":"106","author":"Liu","year":"2021","journal-title":"Plant J."},{"key":"B21","doi-asserted-by":"publisher","DOI":"10.1186\/s13059-014-0550-8","article-title":"Moderated estimation of fold change and dispersion for Rna-Seq data with Deseq2.","volume":"15","author":"Love","year":"2014","journal-title":"Genome Biol."},{"key":"B22","doi-asserted-by":"publisher","DOI":"10.3390\/ijms19123900","article-title":"Chloroplasts at the crossroad of photosynthesis, pathogen infection and plant defense.","volume":"19","author":"Lu","year":"2018","journal-title":"Int. J. Mol. Sci."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1109.e","DOI":"10.1016\/j.cell.2020.07.020","article-title":"A defense pathway linking plasma membrane and chloroplasts and co-opted by pathogens.","volume":"182","author":"Medina-Puche","year":"2020","journal-title":"Cell"},{"key":"B24","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1111\/mpp.12081","article-title":"Quantitative transcriptional changes associated with chlorosis severity in mosaic leaves of tobacco plants infected with Cucumber Mosaic Virus.","volume":"15","author":"Mochizuki","year":"","journal-title":"Mol. Plant Pathol."},{"key":"B25","doi-asserted-by":"publisher","first-page":"292","DOI":"10.1016\/j.virol.2014.04.010","article-title":"Coat protein mutations in an attenuated cucumber mosaic virus encoding mutant 2b protein that lacks rna silencing suppressor activity induces chlorosis with photosynthesis gene repression and chloroplast abnormalities in infected tobacco plants.","author":"Mochizuki","year":"","journal-title":"Virology."},{"key":"B26","doi-asserted-by":"publisher","first-page":"435","DOI":"10.2174\/1389203716666150330125215","article-title":"Role of various hormones in photosynthetic responses of green plants under environmental stresses.","volume":"16","author":"Poonam","year":"2015","journal-title":"Curr. Protein Pept. Sci."},{"key":"B27","doi-asserted-by":"publisher","DOI":"10.1101\/pdb.prot5439","article-title":"Purification of Rna using trizol (tri reagent).","volume":"2010","author":"Rio","year":"2010","journal-title":"Cold Spring Harb. Protoc."},{"key":"B28","doi-asserted-by":"publisher","first-page":"669","DOI":"10.1111\/j.1462-5822.2012.01749.x","article-title":"A Bacterial cysteine protease effector protein interferes with photosynthesis to suppress plant innate immune responses.","volume":"14","author":"Rodr\u00edguez-Herva","year":"2012","journal-title":"Cell Microbiol."},{"key":"B29","doi-asserted-by":"publisher","first-page":"1388","DOI":"10.1073\/pnas.1715556115","article-title":"A virus-targeted plant receptor-like kinase promotes cell-to-cell spread of Rnai.","volume":"115","author":"Rosas-Diaz","year":"2018","journal-title":"Proc. Natl. Acad. Sci. U S A."},{"key":"B30","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1016\/j.tplants.2014.10.002","article-title":"Plant innate immunity\u2013sunny side up?","volume":"20","author":"Stael","year":"2015","journal-title":"Trends Plant Sci."},{"key":"B31","doi-asserted-by":"publisher","first-page":"809","DOI":"10.1016\/j.bbabio.2015.05.008","article-title":"Translational regulation in chloroplasts for development and homeostasis.","volume":"1847","author":"Sun","year":"2015","journal-title":"Biochim. Biophys. Acta"},{"key":"B32","doi-asserted-by":"publisher","first-page":"1408","DOI":"10.4161\/psb.6.9.16967","article-title":"The autophagy gene, Atg18a, plays a negative role in powdery mildew resistance and mildew-induced cell death in Arabidopsis.","volume":"6","author":"Wang","year":"2011","journal-title":"Plant Signal Behav."},{"key":"B33","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-019-13487-6","article-title":"An effector protein of the wheat stripe rust fungus targets chloroplasts and suppresses chloroplast function.","volume":"10","author":"Xu","year":"2019","journal-title":"Nat. Commun."},{"key":"B34","doi-asserted-by":"publisher","DOI":"10.3389\/fpls.2021.637853","article-title":"Chloroplast: the emerging battlefield in plant-microbe interactions.","volume":"12","author":"Yang","year":"2021","journal-title":"Front. Plant Sci."},{"key":"B35","doi-asserted-by":"publisher","first-page":"47","DOI":"10.3969\/j.issn.2095-1736.2006.01.015","article-title":"Improvement of traditional paraffin section preparation methods.","volume":"23","author":"Yang","year":"2006","journal-title":"J. Biol."},{"key":"B36","doi-asserted-by":"publisher","first-page":"5","DOI":"10.3969\/j.issn.1002-3186","article-title":"Improvement and comparison with different resins of madding ultrathin section for the transmission electron microscope specimen-making.","volume":"28","author":"Yang","year":"2013","journal-title":"J. Beijing Univ. Agricult."},{"key":"B37","doi-asserted-by":"publisher","DOI":"10.1038\/nplants.2015.74","article-title":"Chloroplasts play a central role in plant defence and are targeted by pathogen effectors.","volume":"1","author":"Zabala","year":"2015","journal-title":"Nat. Plants"},{"key":"B38","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1104\/pp.112.202846","article-title":"Lipid profiling of the Arabidopsis hypersensitive response reveals specific lipid peroxidation and fragmentation processes: biogenesis of pimelic and azelaic acid.","volume":"160","author":"Zoeller","year":"2012","journal-title":"Plant Physiol."}],"container-title":["Frontiers in Plant Science"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2022.928040\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,7,12]],"date-time":"2022-07-12T13:33:06Z","timestamp":1657632786000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fpls.2022.928040\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,7,12]]},"references-count":38,"alternative-id":["10.3389\/fpls.2022.928040"],"URL":"https:\/\/doi.org\/10.3389\/fpls.2022.928040","relation":{},"ISSN":["1664-462X"],"issn-type":[{"value":"1664-462X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,7,12]]},"article-number":"928040"}}