SEGS-1 episomes generated during cassava mosaic disease enhance disease severity

Cassava is an important root crop that is produced by smallholder farmers across Sub-Saharan Africa. Cassava mosaic disease (CMD), which is caused by a group of cassava mosaic begomoviruses (CMBs), is one of the most devastating diseases of cassava. A previous study showed that SEGS-1 (sequences enh...

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Main Authors: Evangelista Chiunga, Catherine D. Aimone, Cyprian Rajabu, Mary M. Dallas, Joseph Ndunguru, José T. Ascencio-Ibáñez, Elijah M. Ateka, Linda Hanley-Bowdoin
Format: Article
Language:English
Published: Frontiers Media S.A. 2025-01-01
Series:Frontiers in Plant Science
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Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2024.1469045/full
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author Evangelista Chiunga
Evangelista Chiunga
Evangelista Chiunga
Catherine D. Aimone
Cyprian Rajabu
Mary M. Dallas
Joseph Ndunguru
José T. Ascencio-Ibáñez
Elijah M. Ateka
Linda Hanley-Bowdoin
author_facet Evangelista Chiunga
Evangelista Chiunga
Evangelista Chiunga
Catherine D. Aimone
Cyprian Rajabu
Mary M. Dallas
Joseph Ndunguru
José T. Ascencio-Ibáñez
Elijah M. Ateka
Linda Hanley-Bowdoin
author_sort Evangelista Chiunga
collection DOAJ
description Cassava is an important root crop that is produced by smallholder farmers across Sub-Saharan Africa. Cassava mosaic disease (CMD), which is caused by a group of cassava mosaic begomoviruses (CMBs), is one of the most devastating diseases of cassava. A previous study showed that SEGS-1 (sequences enhancing geminivirus symptoms), which occur both in the cassava genome and as episomes during CMD, can increase CMD disease severity and overcome host resistance. In this report, we examined the effects of exogenously applied SEGS-1 on the incidence of CMB infection, symptom severity, and viral DNA copy number in five cassava cultivars that ranged from highly susceptible to highly resistant to CMD. These studies revealed that the effect of SEGS-1 is cultivar dependent. Susceptible cultivars developed severe CMD with or without exogenous SEGS-1, while exogenous SEGS-1 increased disease severity in cultivars carrying CMD2 resistance, which is conferred by a single locus, but not CMD1 resistance, which is polygenic. Analysis of infected plants in the absence of exogenous SEGS-1 revealed that some, but not all, cultivars form SEGS-1 episomes during CMD. The presence of endogenous SEGS-1 episomes in TME14, a CMD2 resistant cultivar, correlated with CMD severity. In contrast, TME3, a closely related CMD2 cultivar, did not produce endogenous SEGS-1 episomes and was more resistance than TME14. The different capacities of TME3 and TME14 to form SEGS-1 episomes is unlikely due to sequence differences in and around their genomic SEGS-1 loci. The functional regions of SEGS-1 were mapped using TME3 to sequences flanking the episome junction, but the junction itself was not required for activity. All cassava cultivars have SEGS-1 sequences in their genomes that have the potential to negatively impact the development of stable CMD resistance by cassava breeding programs.
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publisher Frontiers Media S.A.
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spelling doaj-art-5eff46375e8543da82ce67db44dba44c2025-01-22T11:08:20ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2025-01-011510.3389/fpls.2024.14690451469045SEGS-1 episomes generated during cassava mosaic disease enhance disease severityEvangelista Chiunga0Evangelista Chiunga1Evangelista Chiunga2Catherine D. Aimone3Cyprian Rajabu4Mary M. Dallas5Joseph Ndunguru6José T. Ascencio-Ibáñez7Elijah M. Ateka8Linda Hanley-Bowdoin9Department of Horticulture, Jomo Kenyatta University of Agriculture and Technology, Nairobi, KenyaDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesTanzania Agricultural Research Institute (TARI)-Mikocheni, Dar es Salaam, TanzaniaDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesTanzania Plant Health and Pesticide Authority, Arusha, TanzaniaDepartment of Molecular and Structural Biochemistry, North Carolina State University, Raleigh, NC, United StatesDepartment of Horticulture, Jomo Kenyatta University of Agriculture and Technology, Nairobi, KenyaDepartment of Plant and Microbial Biology, North Carolina State University, Raleigh, NC, United StatesCassava is an important root crop that is produced by smallholder farmers across Sub-Saharan Africa. Cassava mosaic disease (CMD), which is caused by a group of cassava mosaic begomoviruses (CMBs), is one of the most devastating diseases of cassava. A previous study showed that SEGS-1 (sequences enhancing geminivirus symptoms), which occur both in the cassava genome and as episomes during CMD, can increase CMD disease severity and overcome host resistance. In this report, we examined the effects of exogenously applied SEGS-1 on the incidence of CMB infection, symptom severity, and viral DNA copy number in five cassava cultivars that ranged from highly susceptible to highly resistant to CMD. These studies revealed that the effect of SEGS-1 is cultivar dependent. Susceptible cultivars developed severe CMD with or without exogenous SEGS-1, while exogenous SEGS-1 increased disease severity in cultivars carrying CMD2 resistance, which is conferred by a single locus, but not CMD1 resistance, which is polygenic. Analysis of infected plants in the absence of exogenous SEGS-1 revealed that some, but not all, cultivars form SEGS-1 episomes during CMD. The presence of endogenous SEGS-1 episomes in TME14, a CMD2 resistant cultivar, correlated with CMD severity. In contrast, TME3, a closely related CMD2 cultivar, did not produce endogenous SEGS-1 episomes and was more resistance than TME14. The different capacities of TME3 and TME14 to form SEGS-1 episomes is unlikely due to sequence differences in and around their genomic SEGS-1 loci. The functional regions of SEGS-1 were mapped using TME3 to sequences flanking the episome junction, but the junction itself was not required for activity. All cassava cultivars have SEGS-1 sequences in their genomes that have the potential to negatively impact the development of stable CMD resistance by cassava breeding programs.https://www.frontiersin.org/articles/10.3389/fpls.2024.1469045/fullcassava mosaic begomoviruscassava mosaic diseaseCMDSEGS-1resistance
spellingShingle Evangelista Chiunga
Evangelista Chiunga
Evangelista Chiunga
Catherine D. Aimone
Cyprian Rajabu
Mary M. Dallas
Joseph Ndunguru
José T. Ascencio-Ibáñez
Elijah M. Ateka
Linda Hanley-Bowdoin
SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
Frontiers in Plant Science
cassava mosaic begomovirus
cassava mosaic disease
CMD
SEGS-1
resistance
title SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
title_full SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
title_fullStr SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
title_full_unstemmed SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
title_short SEGS-1 episomes generated during cassava mosaic disease enhance disease severity
title_sort segs 1 episomes generated during cassava mosaic disease enhance disease severity
topic cassava mosaic begomovirus
cassava mosaic disease
CMD
SEGS-1
resistance
url https://www.frontiersin.org/articles/10.3389/fpls.2024.1469045/full
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