Modulation of key sterol-related genes of Nicotiana benthamiana by phosphite treatment during infection with Phytophthora cinnamomi
Aayushree Kharel


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Abstract
Phytophthora cinnamomi is a globally destructive pathogen causing disease in over 5000 plant species. As sterol auxotrophs, Phytophthora species rely on host-derived phytosterols for reproduction, yet the effects of pathogen infection on plant sterol biosynthesis remains unclear. We utilised a soil-free plant growth system to analyze the impacts of P. cinnamomi on Nicotiana benthamiana roots, a new model for studying P. cinnamomi–plant root interactions. Our results show that P. cinnamomi successfully infected all ecotypes tested, but infection was inhibited by the systemic chemical, phosphite. While phosphite is traditionally associated with the activation of plant defence mechanisms, we show that phosphite also modulates plant immune receptors and phytosterol biosynthesis. qPCR analyses revealed a two-fold upregulation of the N. benthamiana elicitin receptor, Responsive to Elicitins (REL), and its co-receptor, suppressor of BIR1-1 (SOBIR) during P. cinnamomi infection when compared with infected, phosphite-treated plants. Furthermore, key genes related to plant sterol biosynthesis were upregulated in their expression during pathogen infection but were suppressed in phosphite-treated and infected plants. Notably, the cytochrome P450 family 710 (CYP710A) gene encoding a C22-sterol desaturase, involved in stigmasterol production, a phytosterol known to be linked to plant susceptibility to pathogens, was downregulated in phosphite-treated plants, independent of infection status. These findings reveal novel insights into the role of phosphite in modulating plant immune responses and sterol metabolism, with potential in managing diseases caused by P. cinnamomi.
Keywords: elicitin receptor, Nicotiana benthamiana, phosphite, Phytophthora cinnamomi, plant-pathogen interactions, soil-free plant growth system, sterol metabolism, sterol-related genes.
References
Aberton MJ, Wilson BA, Cahill DM (1999) The use of potassium phosphonate to control Phytophthora cinnamomi in native vegetation at Anglesea, Victoria. Australasian Plant Pathology 28, 225-234.
| Crossref | Google Scholar |
Adachi H, Nakano T, Miyagawa N, Ishihama N, Yoshioka M, Katou Y, Yaeno T, Shirasu K, Yoshioka H (2015) WRKY transcription factors phosphorylated by MAPK regulate a plant immune NADPH oxidase in Nicotiana benthamiana. The Plant Cell 27(9), 2645-2663.
| Crossref | Google Scholar | PubMed |
Akinsanmi O, Neal J, Drenth A, Topp B (2017) Characterization of accessions and species of Macadamia to stem infection by Phytophthora cinnamomi. Plant Pathology 66(2), 186-193.
| Crossref | Google Scholar |
Allardyce JA, Rookes JE, Cahill DM (2012) Defining plant resistance to Phytophthora cinnamomi: a standardized approach to assessment. Journal of Phytopathology 160(6), 269-276.
| Crossref | Google Scholar |
Anderson JM, Pegg KG, Scott C, Drenth A (2012) Phosphonate applied as a pre-plant dip controls Phytophthora cinnamomi root and heart rot in susceptible pineapple hybrids. Australasian Plant Pathology 41, 59-68.
| Crossref | Google Scholar |
Andronis CE, Jacques S, Lipscombe R, Tan K-C (2022) Comparative sub-cellular proteome analyses reveals metabolic differentiation and production of effector-like molecules in the dieback phytopathogen Phytophthora cinnamomi. Journal of Proteomics 269, 104725.
| Crossref | Google Scholar | PubMed |
Andronis CE, Jacques S, Lopez-Ruiz FJ, Lipscombe R, Tan K-C (2024) Proteomic analysis revealed that the oomyceticide phosphite exhibits multi-modal action in an oomycete pathosystem. Journal of Proteomics 301, 105181.
| Crossref | Google Scholar | PubMed |
Atsumi G, Kagaya U, Tabayashi N, Matsumura T (2018) Analysis of the mechanisms regulating the expression of isoprenoid biosynthesis genes in hydroponically-grown Nicotiana benthamiana plants using virus-induced gene silencing. Scientific Reports 8(1), 14804.
| Crossref | Google Scholar | PubMed |
Bally J, Jung H, Mortimer C, Naim F, Philips JG, Hellens R, Bombarely A, Goodin MM, Waterhouse PM (2018) The rise and rise of Nicotiana benthamiana: a plant for all reasons. Annual Review of Phytopathology 56(1), 405-426.
| Crossref | Google Scholar |
Balmer D, Mauch-Mani B (2013) More beneath the surface? Root versus shoot antifungal plant defenses. Frontiers in Plant Science 4, 256.
| Crossref | Google Scholar |
Belisle RJ, McKee B, Hao W, Crowley M, Arpaia ML, Miles TD, Adaskaveg JE, Manosalva P (2019) Phenotypic characterization of genetically distinct Phytophthora cinnamomi isolates from avocado. Phytopathology 109(3), 384-394.
| Crossref | Google Scholar | PubMed |
Benton JM, Cobb AH (1997) The modification of phytosterol profiles and in vitro photosynthetic electron transport of Galium aparine L. (cleavers) treated with the fungicide, epoxiconazole. Plant Growth Regulation 22, 93-100.
| Crossref | Google Scholar |
Bouvier-Naveݩ P, Berna A, Noiriel A, Compagnon V, Carlsson AS, Banas A, Stymne S, Schaller H (2010) Involvement of the phospholipid sterol acyltransferase1 in plant sterol homeostasis and leaf senescence. Plant Physiology 152(1), 107-119.
| Crossref | Google Scholar |
Brasier C, Scanu B, Cooke D, Jung T (2022) Phytophthora: an ancient, historic, biologically and structurally cohesive and evolutionarily successful generic concept in need of preservation. IMA Fungus 13(1), 12.
| Crossref | Google Scholar | PubMed |
Burciaga-Monge A, López-Tubau JM, Laibach N, Deng C, Ferrer A, Altabella T (2022) Effects of impaired steryl ester biosynthesis on tomato growth and developmental processes. Frontiers in Plant Science 13, 984100.
| Crossref | Google Scholar | PubMed |
Burgess TI, Scott JK, Mcdougall KL, Stukely MJC, Crane C, Dunstan WA, Brigg F, Andjic V, White D, Rudman T, Arentz F, Ota N, Hardy GESJ (2017) Current and projected global distribution of Phytophthora cinnamomi, one of the world’s worst plant pathogens. Global Change Biology 23(4), 1661-1674.
| Crossref | Google Scholar | PubMed |
Burra DD, Berkowitz O, Hedley PE, Morris J, Resjö S, Levander F, Liljeroth E, Andreasson E, Alexandersson E (2014) Phosphite-induced changes of the transcriptome and secretome in Solanum tuberosum leading to resistance against Phytophthora infestans. BMC Plant Biology 14, 254.
| Crossref | Google Scholar |
Busquets A, Keim V, Closa M, Del Arco A, Boronat A, Arró M, Ferrer A (2008) Arabidopsis thaliana contains a single gene encoding squalene synthase. Plant Molecular Biology 67, 25-36.
| Crossref | Google Scholar | PubMed |
Cahill D, Legge N, Grant B, Weste G (1989) Cellular and histological changes induced by Phytophthora cinnamomi in a group of plant species ranging from fully susceptible to fully resistant. Phytopathology 79(4), 417-424.
| Crossref | Google Scholar |
Cahill DM, Rookes JE, Wilson BA, Gibson L, McDougall KL (2008) Phytophthora cinnamomi and Australia’s biodiversity: impacts, predictions and progress towards control. Australian Journal of Botany 56(4), 279-310.
| Crossref | Google Scholar |
Cauz-Santos LA, Dodsworth S, Samuel R, Christenhusz MJM, Patel D, Shittu T, Jakob A, Paun O, Chase MW (2022) Genomic insights into recent species divergence in Nicotiana benthamiana and natural variation in Rdr1 gene controlling viral susceptibility. The Plant Journal 111(1), 7-18.
| Crossref | Google Scholar | PubMed |
Chaparro-Garcia A, Wilkinson RC, Gimenez-Ibanez S, Findlay K, Coffey MD, Zipfel C, Rathjen JP, Kamoun S, Schornack S (2011) The receptor-like kinase SERK3/BAK1 is required for basal resistance against the late blight pathogen Phytophthora infestans in Nicotiana benthamiana. PLoS ONE 6(1), e16608.
| Crossref | Google Scholar | PubMed |
Chappell J, VonLanken C, Vögeli U (1991) Elicitor-inducible 3-hydroxy-3-methylglutaryl coenzyme a reductase activity is required for sesquiterpene accumulation in tobacco cell suspension cultures. Plant Physiology 97(2), 693-698.
| Crossref | Google Scholar | PubMed |
Chase MW, Cauz-Santos LA, Dodsworth S, Christenhusz MJM (2022) Taxonomy of the Australian Nicotiana benthamiana complex (Nicotiana section Suaveolentes; Solanaceae): five species, four newly described, with distinct ranges and morphologies. Australian Systematic Botany 35(5), 345-363.
| Crossref | Google Scholar |
Chen Z, Liu F, Zeng M, Wang L, Liu H, Sun Y, Wang L, Zhang Z, Chen Z, Xu Y, Zhang M, Xia Y, Ye W, Dong S, Govers F, Wang Y, Wang Y (2023) Convergent evolution of immune receptors underpins distinct elicitin recognition in closely related Solanaceous plants. The Plant Cell 35(4), 1186-1201.
| Crossref | Google Scholar | PubMed |
Coelho AC, Pires R, Schütz G, Santa C, Manadas B, Pinto P (2021) Disclosing proteins in the leaves of cork oak plants associated with the immune response to Phytophthora cinnamomi inoculation in the roots: a long-term proteomics approach. PLoS ONE 16(1), e0245148.
| Crossref | Google Scholar | PubMed |
Crone M, McComb JA, O’Brien PA, Hardy GESJ (2013) Survival of Phytophthora cinnamomi as oospores, stromata, and thick-walled chlamydospores in roots of symptomatic and asymptomatic annual and herbaceous perennial plant species. Fungal Biology 117(2), 112-123.
| Crossref | Google Scholar | PubMed |
De Coninck B, Timmermans P, Vos C, Cammue BPA, Kazan K (2015) What lies beneath: belowground defense strategies in plants. Trends in Plant Science 20(2), P91-101.
| Crossref | Google Scholar |
Der C, Courty P-E, Recorbet G, Wipf D, Simon-Plas F, Gerbeau-Pissot P (2024) Sterols, pleiotropic players in plant–microbe interactions. Trends in Plant Science 29(5), 524-534.
| Crossref | Google Scholar | PubMed |
Derevnina L, Dagdas YF, De la Concepcion JC, Bialas A, Kellner R, Petre B, Domazakis E, Du J, Wu C-H, Lin X, Aguilera-Galvez C, Cruz-Mireles N, Vleeshouwers VGAA, Kamoun S (2016) Nine things to know about elicitins. New Phytologist 212(4), 888-895.
| Crossref | Google Scholar | PubMed |
Dokládal L, Obořil M, Stejskal K, Zdráhal Z, Ptáčková N, Chaloupkova R, Damborský J, Kašparovský T, Jeandroz S, Žd’árská M, Lochman J (2012) Physiological and proteomic approaches to evaluate the role of sterol binding in elicitin-induced resistance. Journal of Experimental Botany 63(5), 2203-2215.
| Crossref | Google Scholar | PubMed |
Domazakis E, Wouters D, Visser RGF, Kamoun S, Joosten MHAJ, Vleeshouwers VGAA (2018) The ELR-SOBIR1 complex functions as a two-component receptor-like kinase to mount defense against Phytophthora infestans. Molecular Plant-Microbe Interactions 31(8), 795-802.
| Crossref | Google Scholar | PubMed |
Du J, Verzaux E, Chaparro-Garcia A, Bijsterbosch G, Keizer LCP, Zhou J, Liebrand TWH, Xie C, Govers F, Robatzek S, van der Vossen EAG, Jacobsen E, Visser RGF, Kamoun S, Vleeshouwers , VGAA (2015) Elicitin recognition confers enhanced resistance to Phytophthora infestans in potato. Nature Plants 1(4), 15034.
| Crossref | Google Scholar |
Du Y, Fu X, Chu Y, Wu P, Liu Y, Ma L, Tian H, Zhu B (2022) Biosynthesis and the roles of plant sterols in development and stress responses. International Journal of Molecular Sciences 23(4), 2332.
| Crossref | Google Scholar | PubMed |
Dundas SJ, Hardy GESJ, Fleming PA (2016) The plant pathogen Phytophthora cinnamomi influences habitat use by the obligate nectarivore honey possum (Tarsipes rostratus). Australian Journal of Zoology 64(2), 122-131.
| Crossref | Google Scholar |
Enfissi EMA, Fraser PD, Lois L-M, Boronat A, Schuch W, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of health-promoting isoprenoids in tomato. Plant Biotechnology Journal 3(1), 17-27.
| Crossref | Google Scholar | PubMed |
Engelbrecht J, Van den Berg N (2013) Expression of defence-related genes against Phytophthora cinnamomi in five avocado rootstocks. South African Journal of Science 109(11/12), 8.
| Crossref | Google Scholar |
Eshraghi L, Anderson J, Aryamanesh N, Shearer B, McComb J, Hardy GESJ, O’Brien PA (2011) Phosphite primed defence responses and enhanced expression of defence genes in Arabidopsis thaliana infected with Phytophthora cinnamomi. Plant Pathology 60(6), 1086-1095.
| Crossref | Google Scholar |
Evangelisti E, Govers F (2024) Roadmap to success: how oomycete plant pathogens invade tissues and deliver effectors. Annual Review of Microbiology 78, 493-512.
| Crossref | Google Scholar |
Evangelisti E, Gogleva A, Hainaux T, Doumane M, Tulin F, Quan C, Yunusov T, Floch K, Schornack S (2017) Time-resolved dual transcriptomics reveal early induced Nicotiana benthamiana root genes and conserved infection-promoting Phytophthora palmivora effectors. BMC Biology 15, 39.
| Crossref | Google Scholar |
Fabro G, Di Rienzo JA, Voigt CA, Savchenko T, Dehesh K, Somerville S, Alvarez ME (2008) Genome-wide expression profiling Arabidopsis at the stage of Golovinomyces cichoracearum haustorium formation. Plant Physiology 146(3), 1421-1439.
| Crossref | Google Scholar | PubMed |
Fernandes P, Machado H, Silva MdC, Costa RL (2021) A histopathological study reveals new insights into responses of chestnut (Castanea spp.) to root infection by Phytophthora cinnamomi. Phytopathology 111(2), 345-355.
| Crossref | Google Scholar | PubMed |
Ferrer A, Altabella T, Arró M, Boronat A (2017) Emerging roles for conjugated sterols in plants. Progress in Lipid Research 67, 27-37.
| Crossref | Google Scholar | PubMed |
Fröschel C (2021) In-depth evaluation of root infection systems using the vascular fungus Verticillium longisporum as soil-borne model pathogen. Plant Methods 17(1), 57.
| Crossref | Google Scholar | PubMed |
Gao H, Ge W, Bai L, Zhang T, Zhao L, Li J, Shen J, Xu N, Zhang H, Wang G, Lin X (2023) Proteomic analysis of leaves and roots during drought stress and recovery in Setaria italica L. Frontiers in Plant Science 14, 1240164.
| Crossref | Google Scholar | PubMed |
Gómez-Merino FC, Trejo-Téllez LI (2015) Biostimulant activity of phosphite in horticulture. Scientia Horticulturae 196, 82-90.
| Crossref | Google Scholar |
Griebel T, Zeier J (2010) A role for β-sitosterol to stigmasterol conversion in plant–pathogen interactions. The Plant Journal 63(2), 254-268.
| Crossref | Google Scholar | PubMed |
Gunning T, Cahill DM (2009) A soil-free plant growth system to facilitate analysis of plant pathogen interactions in roots. Journal of Phytopathology 157(7–8), 497-501.
| Crossref | Google Scholar |
Gunning TK, Conlan XA, Parker RM, Dyson GA, Adams MJ, Barnett NW, Cahill DM (2013) Profiling of secondary metabolites in blue lupin inoculated with Phytophthora cinnamomi following phosphite treatment. Functional Plant Biology 40(11), 1089-1097.
| Crossref | Google Scholar | PubMed |
Hardham AR, Blackman LM (2018) Phytophthora cinnamomi. Molecular Plant Pathology 19(2), 260-285.
| Crossref | Google Scholar |
Hardy GESJ, Barrett S, Shearer BL (2001) The future of phosphite as a fungicide to control the soilborne plant pathogen Phytophthora cinnamomi in natural ecosystems. Australasian Plant Pathology 30, 133-139.
| Crossref | Google Scholar |
Harker M, Holmberg N, Clayton JC, Gibbard CL, Wallace AD, Rawlins S, Hellyer SA, Lanot A, Safford R (2003) Enhancement of seed phytosterol levels by expression of an N-terminal truncated Hevea brasiliensis (rubber tree) 3-hydroxy-3-methylglutaryl-CoA reductase. Plant Biotechnology Journal 1(2), 113-121.
| Crossref | Google Scholar | PubMed |
He H, Xu T, Cao F, Xu Y, Dai T, Liu T (2024) PcAvh87, a virulence essential RxLR effector of Phytophthora cinnamomi suppresses host defense and induces cell death in plant nucleus. Microbiological Research 286, 127789.
| Crossref | Google Scholar | PubMed |
Horta M, Sousa N, Coelho AC, Neves D, Cravador A (2008) In vitro and in vivo quantification of elicitin expression in Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 73(1–3), 48-57.
| Crossref | Google Scholar |
Huang WR, Joosten MHAJ (2024) Immune signaling: receptor-like proteins make the difference. Trends in Plant Science 30(1), 54-68.
| Crossref | Google Scholar | PubMed |
Huang WRH, Schol C, Villanueva SL, Heidstra R, Joosten MHAJ (2021) Knocking out SOBIR1 in Nicotiana benthamiana abolishes functionality of transgenic receptor-like protein Cf-4. Plant Physiology 185(2), 290-294.
| Crossref | Google Scholar | PubMed |
Islam MT, Rookes JE, Cahill DM (2017) Active defence by an Australian native host, Lomandra longifolia, provides resistance against Phytophthora cinnamomi. Functional Plant Biology 44, 386-399.
| Crossref | Google Scholar | PubMed |
Islam MT, Hussain HI, Russo R, Chambery A, Amoresano A, Schallmey A, Oßwald W, Nadiminti PP, Cahill DM (2019) Functional analysis of elicitins and identification of cell wall proteins in Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 107, 21-32.
| Crossref | Google Scholar |
Islam MT, Gan HM, Ziemann M, Hussain HI, Arioli T, Cahill D (2020) Phaeophyceaean (brown algal) extracts activate plant defense systems in Arabidopsis thaliana challenged with Phytophthora cinnamomi. Frontiers in Plant Science 11, 852.
| Crossref | Google Scholar | PubMed |
Jackson TJ, Burgess TI, Colquhoun I, Hardy GESJ (2000) Action of the fungicide phosphite on Eucalyptus marginata inoculated with Phytophthora cinnamomi. Plant Pathology 49(1), 147-154.
| Crossref | Google Scholar |
Kamoun S, Furzer O, Jones JD, Judelson HS, Ali GS, Dalio RJD, Roy SG, Schena L, Zambounis A, Panabières F, Cahill D, Ruocco M, Figueiredo A, Chen X-R, Hylvey J, Stam R, Lamour K, Gijzen M, Tyler BM, Grünwald NJ, Mukhtar MS, Tomé DF, Tör M, Van Den Ackerveken G, McDowell J, Daayf F, Fry WE, Lindqvist-Kreuze H, Meijer HJG, Petre B, Ristaino J, Yoshida K, Birch PRJ, Govers F (2015) The top 10 oomycete pathogens in molecular plant pathology. Molecular Plant Pathology 16(4), 413-434.
| Crossref | Google Scholar | PubMed |
Kharel A, Adcock J, Ziemann M, Rookes J, Cahill D (2024a) Sterol complex visualisation in Phytophthora cinnamomi and expression analysis of genes involved in sterol sensing, recruitment and conversion. Physiological and Molecular Plant Pathology 133, 102371.
| Crossref | Google Scholar |
Kharel A, Rookes J, Ziemann M, Cahill D (2024b) Viable protoplast isolation, organelle visualization and transformation of the globally distributed plant pathogen Phytophthora cinnamomi. Protoplasma 261, 1073-1092.
| Crossref | Google Scholar |
Kim Y-J, Lee OR, Oh JY, Jang M-G, Yang D-C (2014) Functional analysis of 3-hydroxy-3-methylglutaryl coenzyme a reductase encoding genes in triterpene saponin-producing ginseng. Plant Physiology 165(1), 373-387.
| Crossref | Google Scholar | PubMed |
King M, Reeve W, Van der Hoek MB, Williams N, McComb J, O’Brien PA, Hardy GESJ (2010) Defining the phosphite-regulated transcriptome of the plant pathogen Phytophthora cinnamomi. Molecular Genetics and Genomics 284, 425-435.
| Crossref | Google Scholar | PubMed |
Kopischke M, Westphal L, Schneeberger K, Clark R, Ossowski S, Wewer V, Fuchs R, Landtag J, Hause G, Dörmann P, Lipka V, Weigel D, Schulze-Lefert P, Scheel D, Rosahl S (2013) Impaired sterol ester synthesis alters the response of Arabidopsis thaliana to Phytophthora infestans. The Plant Journal 73(3), 456-468.
| Crossref | Google Scholar | PubMed |
Li W, Liu W, Wei H, He Q, Chen J, Zhang B, Zhu S (2014) Species-specific expansion and molecular evolution of the 3-hydroxy-3-methylglutaryl coenzyme a reductase (HMGR) gene family in plants. PLoS ONE 9(4), e94172.
| Crossref | Google Scholar | PubMed |
Liao P, Lung S-C, Chan WL, Bach TJ, Lo C, Chye M-L (2020) Overexpression of HMG-CoA synthase promotes Arabidopsis root growth and adversely affects glucosinolate biosynthesis. Journal of Experimental Botany 71(1), 272-289.
| Crossref | Google Scholar | PubMed |
Lin X, Olave-Achury A, Heal R, Pais M, Witek K, Ahn H-K, Zhao H, Bhanvadia S, Karki HS, Song T, Wu C-H, Adachi H, Kamoun S, Vleeshouwers VGAA, Jones JDG (2022) A potato late blight resistance gene protects against multiple Phytophthora species by recognizing a broadly conserved RXLR-WY effector. Molecular Plant 15(9), 1457-1469.
| Crossref | Google Scholar | PubMed |
Liu D, Shi L, Han C, Yu J, Li D, Zhang Y (2012) Validation of reference genes for gene expression studies in virus-infected Nicotiana benthamiana using quantitative real-time PCR. PLoS ONE 7(9), e46451.
| Crossref | Google Scholar | PubMed |
Liu L, Sonbol F-M, Huot B, Gu Y, Withers J, Mwimba M, Yao J, He SY, Dong X (2016) Salicylic acid receptors activate jasmonic acid signalling through a non-canonical pathway to promote effector-triggered immunity. Nature Communications 7(1), 13099.
| Crossref | Google Scholar |
Machinandiarena MF, Lobato MC, Feldman ML, Daleo GR, Andreu AB (2012) Potassium phosphite primes defense responses in potato against Phytophthora infestans. Journal of Plant Physiology 169(14), 1417-1424.
| Crossref | Google Scholar | PubMed |
Massoud K, Barchietto T, Le Rudulier T, Pallandre L, Didierlaurent L, Garmier M, Ambard-Bretteville F, Seng J-M, Saindrenan P (2012) Dissecting phosphite-induced priming in Arabidopsis infected with Hyaloperonospora arabidopsidis. Plant Physiology 159(1), 286-298.
| Crossref | Google Scholar | PubMed |
McDougall KL, Barrett S, Velzeboer R, Cahill DM, Rudman T (2024) Evaluating the risk to Australia’s flora from Phytophthora cinnamomi. Australian Journal of Botany 72, BT23086.
| Crossref | Google Scholar |
Mohammadi MA, Cheng Y, Aslam M, Jakada BH, Wai MH, Ye K, He X, Luo T, Ye L, Dong C, Hu B, Priyadarshani SVGN, Wang-Pruski G, Qin Y (2021) ROS and oxidative response systems in plants under biotic and abiotic stresses: revisiting the crucial role of phosphite triggered plants defense response. Frontiers in Microbiology 12, 631318.
| Crossref | Google Scholar | PubMed |
Mohammed U, Davis J, Rossall S, Swarup K, Czyzewicz N, Bhosale R, Foulkes J, Murchie EH, Swarup R (2022) Phosphite treatment can improve root biomass and nutrition use efficiency in wheat. Frontiers in Plant Science 13, 1017048.
| Crossref | Google Scholar | PubMed |
Morikawa T, Mizutani M, Aoki N, Watanabe B, Saga H, Saito S, Oikawa A, Suzuki H, Sakurai N, Shibata D, Wadano A, Sakata K, Ohta D (2006) Cytochrome P450 CYP710A encodes the sterol C-22 desaturase in Arabidopsis and tomato. The Plant Cell 18(4), 1008-1022.
| Crossref | Google Scholar | PubMed |
Nes WD (2011) Biosynthesis of cholesterol and other sterols. Chemical Reviews 111(10), 6423-6451.
| Crossref | Google Scholar | PubMed |
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59(2), 368-373.
| Crossref | Google Scholar |
Pérez-Zavala FG, Ojeda-Rivera JO, Herrera-Estrella L, López-Arredondo D (2024) Beneficial effects of phosphite in Arabidopsis thaliana mediated by activation of ABA, SA, and JA biosynthesis and signaling pathways. Plants 13(13), 1873.
| Crossref | Google Scholar | PubMed |
Perez V, Mamdouh AM, Huet J-C, Pernollet J-C, Bompeix G (1995) Enhanced secretion of elicitins by Phytophthora fungi exposed to phosphonate. Cryptogamie. Mycologie 16, 191-194.
| Crossref | Google Scholar |
Phillips D, Grant B, Weste G (1987) Histological changes in the roots of an avocado cultivar, Duke 7, infected with Phytophthora cinnamomi. Cytology and Histology 77(5), 691-698.
| Google Scholar |
Rahier A, Taton M (1997) Fungicides as tools in studying postsqualene sterol synthesis in plants. Pesticide Biochemistry and Physiology 57(1), 1-27.
| Crossref | Google Scholar |
Ranawaka B, An J, Lorenc MT, Jung H, Sulli M, Aprea G, Roden S, Llaca V, Hayashi S, Asadyar L, LeBlanc Z, Ahmed Z, Naim F, de Campos SB, Cooper T, de Felippes FF, Dong P, Zhong S, Garcia-Carpintero V, Orzaez D, Dudley KJ, Bombarely A, Bally J, Winefield C, Waterhouse PM (2023) A multi-omic Nicotiana benthamiana resource for fundamental research and biotechnology. Nature Plants 9, 1558-1571.
| Crossref | Google Scholar | PubMed |
Rasmann S, Agrawal AA (2008) In defense of roots: a research agenda for studying plant resistance to belowground herbivory. Plant Physiology 146(3), 875-880.
| Crossref | Google Scholar | PubMed |
Redondo MÁ, Pérez-Sierra A, Abad-Campos P, Torres L, Solla A, Reig-Armiñana J, García-Breijo F (2015) Histology of Quercus ilex roots during infection by Phytophthora cinnamomi. Trees 29, 1943-1957.
| Crossref | Google Scholar |
Robinson LH, Cahill DM (2003) Ecotypic variation in the response of Arabidopsis thaliana to Phytophthora cinnamomi. Australasian Plant Pathology 32, 53-64.
| Crossref | Google Scholar |
Rodríguez-Romero M, Cardillo E, Santiago R, Pulido F (2022) Susceptibility to Phytophthora cinnamomi of six holm oak (Quercus ilex) provenances: are results under controlled vs. natural conditions consistent? Forest Systems 31(2), e011.
| Crossref | Google Scholar |
Rookes JE, Wright ML, Cahill DM (2008) Elucidation of defence responses and signalling pathways induced in Arabidopsis thaliana following challenge with Phytophthora cinnamomi. Physiological and Molecular Plant Pathology 72(4–6), 151-161.
| Crossref | Google Scholar |
Ruiz Gómez FJ, Navarro-Cerrillo RM, Sánchez-Cuesta R, Pérez-de-Luque A (2015) Histopathology of infection and colonization of Quercus ilex fine roots by Phytophthora cinnamomi. Plant Pathology 64(3), 605-616.
| Crossref | Google Scholar |
Schuster M, Kilaru S, Steinberg G (2024) Azoles activate type I and type II programmed cell death pathways in crop pathogenic fungi. Nature Communications 15(1), 4357.
| Crossref | Google Scholar | PubMed |
Sena K, Crocker E, Vincelli P, Barton C (2018) Phytophthora cinnamomi as a driver of forest change: implications for conservation and management. Forest Ecology and Management 409, 799-807.
| Crossref | Google Scholar |
Shands AC, Xu G, Belisle RJ, Seifbarghi S, Jackson N, Bombarely A, Cano LM, Manosalva PM (2024) Genomic and transcriptomic analyses of Phytophthora cinnamomi reveal complex genome architecture, expansion of pathogenicity factors, and host-dependent gene expression profiles. Frontiers in Microbiology 15, 1341803.
| Crossref | Google Scholar | PubMed |
Shearer BL, Fairman RG (2007) A stem injection of phosphite protects Banksia species and Eucalyptus marginata from Phytophthora cinnamomi for at least four years. Australasian Plant Pathology 36(1), 78-86.
| Crossref | Google Scholar |
Shearer BL, Crane CE, Barrett S, Cochrane A (2007) Phytophthora cinnamomi invasion, a major threatening process to conservation of flora diversity in the South-west Botanical Province of Western Australia. Australian Journal of Botany 55(3), 225-238.
| Crossref | Google Scholar |
Shen D, Chai C, Ma L, Zhang M, Dou D (2016) Comparative RNA-seq analysis of Nicotiana benthamiana in response to Phytophthora parasitica infection. Plant Growth Regulation 80, 59-67.
| Crossref | Google Scholar |
Sinhalagoda C, Wilson MD, Tran SN, Cahill D, Barry KM (2023) Screening native pepper, Tasmannia lanceolata (Poir.) A.C. Smith, for resistance against Phytophthora cinnamomi dieback. Australasian Plant Pathology 52(5), 427-437.
| Crossref | Google Scholar |
Taylor SC, Nadeau K, Abbasi M, Lachance C, Nguyen M, Fenrich J (2019) The ultimate qPCR experiment: producing publication quality, reproducible data the first time. Trends in Biotechnology 37(7), 761-774.
| Crossref | Google Scholar | PubMed |
Valitova J, Renkova A, Beckett R, Minibayeva F (2024) Stigmasterol: an enigmatic plant stress sterol with versatile functions. International Journal of Molecular Sciences 25(15), 8122.
| Crossref | Google Scholar | PubMed |
Wang K, Senthil-Kumar M, Ryu C-M, Kang L, Mysore KS (2012) Phytosterols play a key role in plant innate immunity against bacterial pathogens by regulating nutrient efflux into the apoplast. Plant physiology 158(4), 1789-1802.
| Crossref | Google Scholar | PubMed |
Wang J, Qin Q, Pan J, Sun L, Sun Y, Xue Y, Song K (2019) Transcriptome analysis in roots and leaves of wheat seedlings in response to low-phosphorus stress. Scientific Reports 9(1), 19802.
| Crossref | Google Scholar | PubMed |
Wang W, Liu X, Govers F (2021) The mysterious route of sterols in oomycetes. PLoS Pathogens 17(6), e1009591.
| Crossref | Google Scholar | PubMed |
Wilkinson CJ, Holmes JM, Dell B, Tynan KM, McComb JA, Shearer BL, Colquhoun IJ, Hardy GESJ (2001) Effect of phosphite on in planta zoospore production of Phytophthora cinnamomi. Plant Pathology 50(5), 587-593.
| Crossref | Google Scholar |
Williams N, Hardy GESJ, O’Brien PA (2009) Analysis of the distribution of Phytophthora cinnamomi in soil at a disease site in Western Australia using nested PCR. Forest Pathology 39(2), 95-109.
| Crossref | Google Scholar |
Witek K, Jupe F, Witek AI, Baker D, Clark MD, Jones JD (2016) Accelerated cloning of a potato late blight–resistance gene using RenSeq and SMRT sequencing. Nature Biotechnology 34(6), 656-660.
| Crossref | Google Scholar | PubMed |
Yang X, Tyler BM, Hong C (2017) An expanded phylogeny for the genus Phytophthora. IMA Fungus 8, 355-384.
| Crossref | Google Scholar | PubMed |