Differential Symptomology, Susceptibility, and Titer Dynamics Manifested by Phytoplasma-Infected Periwinkle and Tomato Plants

Overview

Journal Plants (Basel)

Date 2024 Apr 9

PMID 38592808

Authors

Algirdas Ivanauskas

Junichi Inaba

Yan Zhao

Kristi D Bottner-Parker

Wei Wei

Affiliations

Soon will be listed here.

Abstract

Phytoplasmas are intracellular pathogenic bacteria that infect a wide range of plant species, including agriculturally important crops and ornamental trees. However, our understanding of the relationship between symptom severity, disease progression, and phytoplasma concentration remains limited due to the inability to inoculate phytoplasmas mechanically into new plant hosts. The present study investigated phytoplasma titer dynamics and symptom development in periwinkle and tomato, both infected with the same potato purple top (PPT) phytoplasma strain using a small seedling grafting approach. Virescence, phyllody, and witches'-broom (WB) symptoms sequentially developed in periwinkle, while in tomato plants, big bud (BB, a form of phyllody), cauliflower-like inflorescence (CLI), and WB appeared in order. Results from quantitative polymerase chain reaction (qPCR) targeting the PPT phytoplasma's 16S rRNA gene revealed that in both host species, phytoplasma titers differed significantly at different infection stages. Notably, the highest phytoplasma concentration in periwinkles was observed in samples displaying phyllody symptoms, whereas in tomatoes, the titer peaked at the BB stage. Western blot analysis, utilizing an antibody specific to PPT phytoplasma, confirmed substantial phytoplasma presence in samples displaying phyllody and BB symptoms, consistent with the qPCR results. These findings challenge the conventional understanding that phytoplasma infection dynamics result in a higher titer at later stages, such as WB (excessive vegetative growth), rather than in the early stage, such as phyllody (abnormal reproductive growth). Furthermore, the PPT phytoplasma titer was markedly higher in periwinkles than in tomato plants, indicating differing susceptibilities between the hosts. This study reveals distinct host responses to PPT phytoplasma infection, providing valuable insights into phytoplasma titer dynamics and symptom development, with implications for the future management of agricultural disease.

References

Mello A, Yokomi R, Melcher U, Chen J, Fletcher J . Citrus Stubborn Severity Is Associated with Spiroplasma citri Titer But Not with Bacterial Genotype. Plant Dis. 2019; 94(1):75-82. DOI: 10.1094/PDIS-94-1-0075. View

Park C, Bart R, Chern M, Canlas P, Bai W, Ronald P . Overexpression of the endoplasmic reticulum chaperone BiP3 regulates XA21-mediated innate immunity in rice. PLoS One. 2010; 5(2):e9262. PMC: 2822859. DOI: 10.1371/journal.pone.0009262. View

Dutta A, Croll D, McDonald B, Barrett L . Maintenance of variation in virulence and reproduction in populations of an agricultural plant pathogen. Evol Appl. 2021; 14(2):335-347. PMC: 7896723. DOI: 10.1111/eva.13117. View

Wei W, Davis R, Nuss D, Zhao Y . Phytoplasmal infection derails genetically preprogrammed meristem fate and alters plant architecture. Proc Natl Acad Sci U S A. 2013; 110(47):19149-54. PMC: 3839765. DOI: 10.1073/pnas.1318489110. View

Block A, Toruno T, Elowsky C, Zhang C, Steinbrenner J, Beynon J . The Pseudomonas syringae type III effector HopD1 suppresses effector-triggered immunity, localizes to the endoplasmic reticulum, and targets the Arabidopsis transcription factor NTL9. New Phytol. 2013; 201(4):1358-1370. DOI: 10.1111/nph.12626. View

Huang W, MacLean A, Sugio A, Maqbool A, Busscher M, Cho S . Parasitic modulation of host development by ubiquitin-independent protein degradation. Cell. 2021; 184(20):5201-5214.e12. PMC: 8525514. DOI: 10.1016/j.cell.2021.08.029. View

Carminati G, Brusa V, Loschi A, Ermacora P, Martini M . Spatiotemporal and Quantitative Monitoring of the Fate of " Phytoplasma Solani" in Tomato Plants Infected by Grafting. Pathogens. 2021; 10(7). PMC: 8308695. DOI: 10.3390/pathogens10070811. View

Lee I, Davis R, Gundersen-Rindal D . Phytoplasma: phytopathogenic mollicutes. Annu Rev Microbiol. 2000; 54:221-55. DOI: 10.1146/annurev.micro.54.1.221. View

Inaba J, Kim B, Zhao Y, Jansen A, Wei W . The Endoplasmic Reticulum Is a Key Battleground between Phytoplasma Aggression and Host Plant Defense. Cells. 2023; 12(16). PMC: 10453741. DOI: 10.3390/cells12162110. View

10.

Tan Y, Li Q, Zhao Y, Wei H, Wang J, Baker C . Integration of metabolomics and existing omics data reveals new insights into phytoplasma-induced metabolic reprogramming in host plants. PLoS One. 2021; 16(2):e0246203. PMC: 7861385. DOI: 10.1371/journal.pone.0246203. View

11.

Wei W, Davis R, Bauchan G, Zhao Y . New Symptoms Identified in Phytoplasma-Infected Plants Reveal Extra Stages of Pathogen-Induced Meristem Fate-Derailment. Mol Plant Microbe Interact. 2019; 32(10):1314-1323. DOI: 10.1094/MPMI-01-19-0035-R. View

12.

Lee I, Martini M, Marcone C, Zhu S . Classification of phytoplasma strains in the elm yellows group (16SrV) and proposal of 'Candidatus Phytoplasma ulmi' for the phytoplasma associated with elm yellows. Int J Syst Evol Microbiol. 2004; 54(Pt 2):337-347. DOI: 10.1099/ijs.0.02697-0. View

13.

Wei W, Inaba J, Zhao Y, Mowery J, Hammond R . Phytoplasma Infection Blocks Starch Breakdown and Triggers Chloroplast Degradation, Leading to Premature Leaf Senescence, Sucrose Reallocation, and Spatiotemporal Redistribution of Phytohormones. Int J Mol Sci. 2022; 23(3). PMC: 8836287. DOI: 10.3390/ijms23031810. View

14.

MacLean A, Sugio A, Makarova O, Findlay K, Grieve V, Toth R . Phytoplasma effector SAP54 induces indeterminate leaf-like flower development in Arabidopsis plants. Plant Physiol. 2011; 157(2):831-41. PMC: 3192582. DOI: 10.1104/pp.111.181586. View

15.

Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth B, Remm M . Primer3--new capabilities and interfaces. Nucleic Acids Res. 2012; 40(15):e115. PMC: 3424584. DOI: 10.1093/nar/gks596. View

16.

Weintraub P, Beanland L . Insect vectors of phytoplasmas. Annu Rev Entomol. 2005; 51:91-111. DOI: 10.1146/annurev.ento.51.110104.151039. View

17.

Tovi N, Frenk S, Hadar Y, Minz D . Host Specificity and Spatial Distribution Preference of Three Isolates. Front Microbiol. 2019; 9:3263. PMC: 6335278. DOI: 10.3389/fmicb.2018.03263. View

18.

Oshima K, Kakizawa S, Nishigawa H, Jung H, Wei W, Suzuki S . Reductive evolution suggested from the complete genome sequence of a plant-pathogenic phytoplasma. Nat Genet. 2003; 36(1):27-9. DOI: 10.1038/ng1277. View

19.

Wei W, Kakizawa S, Suzuki S, Jung H, Nishigawa H, Miyata S . In planta dynamic analysis of onion yellows phytoplasma using localized inoculation by insect transmission. Phytopathology. 2008; 94(3):244-50. DOI: 10.1094/PHYTO.2004.94.3.244. View

20.

Wang Y, Melzer R, Theissen G . A double-flowered variety of lesser periwinkle (Vinca minor fl. pl.) that has persisted in the wild for more than 160 years. Ann Bot. 2011; 107(9):1445-52. PMC: 3108809. DOI: 10.1093/aob/mcr090. View