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Defense strategies against sweet potato chlorotic stunt and pakakuy virus coinfection unraveled

This study into the response of two Ipomoea batatas (L.) Lam cultivars, Melinda and Tio Joe, to coinfection with sweet potato chlorotic stunt virus (SPCSV) and sweet potato pakakuy virus (SPPV), employed a comprehensive approach encompassing symptomatology, real‐time quantitative polymerase chain re...

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Bibliographic Details
Published in:Crop science 2024-11, Vol.64 (6), p.3438-3460
Main Authors: Kiemo, Francis Wanjohi, Salamon, Pál, Tóth, Zoltán, Szabó, Zoltán
Format: Article
Language:English
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Summary:This study into the response of two Ipomoea batatas (L.) Lam cultivars, Melinda and Tio Joe, to coinfection with sweet potato chlorotic stunt virus (SPCSV) and sweet potato pakakuy virus (SPPV), employed a comprehensive approach encompassing symptomatology, real‐time quantitative polymerase chain reaction, metagenomics, and transcriptomics. SPCSV is a quarantine virus with synergistic effects, which decimate yields. SPPV is the most prevalent DNA virus in sweet potato germplasm, with a tendency to persist in meristems, posing a significant risk for germplasm transfer between territories. Graft inoculation experiments revealed that while Tio Joe remained asymptomatic for 12 weeks and suppressed virus replication, Melinda displayed symptoms early on and exhibited high virus titers. Metagenomic analyses corroborated these observations and confirmed that SPCSV and SPPV were responsible. Transcriptomic analysis unveiled disparities in gene expression between Melinda and Tio Joe. Differential gene expression was heightened and altered in Melinda as the viruses disrupted its gene expression. Its defense strategies, such as inducing abscisic acid signaling, were insufficient to overcome disruptive viral effects like oxidative stress, rendering it susceptible. In contrast, Tio Joe had relatively stable differential gene expression, indicating resistance to SPPV–SPCSV coinfection. Overexpressed genes such as sirtuin, rapid alkalization factor, and nuclear pore anchor triggered quantitative resistance, supported with enriched organelles such as mitochondrion and pathways such as proteasome and cutin, suberine, and wax biosynthesis. Tio Joe maintained its genome integrity and inhibited viral replication by tightly controlling gene expression and preventing reactive oxygen species accumulation. Core Ideas Ipomoea batatas ‘Tio Joe’ resisted sweet potato pakakuy virus–sweet potato chlorotic stunt virus (SPPV–SPCSV) coinfection, while Melinda was susceptible. Tio Joe inhibited viral replication through quantitative resistance and targeted defense responses. Unlike Tio Joe, Melinda was symptomatic and exhibited compatible plant‐virus interactions. Plain Language Summary We investigated how two sweet potato types, Melinda and Tio Joe, responded to coinfection by two viruses, SPPV and SPCSV. As expected, both types induced defense mechanisms against the viruses. Melinda's responses were not strong enough to overcome the infection, leading to virus symptoms such as stunting.
ISSN:0011-183X
1435-0653
DOI:10.1002/csc2.21392