Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance

Background Whiteflies are a global threat to crop yields, including the African subsistence crop cassava ( Manihot esculenta ). Outbreaks of superabundant whitefly populations throughout Eastern and Central Africa in recent years have dramatically increased the pressures of whitefly feeding and viru...

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Main Authors: Nye, Danielle G., Irigoyen, Maria L., Pérez Fons, Laura, Bohorquez-Chaux, Adriana, Hur, Manhoi, Medina-Yerena, Diana, Becerra-Lopez-Lavalle, Luis Augusto, Fraser, Paul D., Walling, Linda L.
Format: Journal Article
Language:Inglés
Published: BioMed Central 2023
Subjects:
Online Access:https://hdl.handle.net/10568/138495
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author Nye, Danielle G.
Irigoyen, Maria L.
Pérez Fons, Laura
Bohorquez-Chaux, Adriana
Hur, Manhoi
Medina-Yerena, Diana
Becerra-Lopez-Lavalle, Luis Augusto
Fraser, Paul D.
Walling, Linda L.
author_browse Becerra-Lopez-Lavalle, Luis Augusto
Bohorquez-Chaux, Adriana
Fraser, Paul D.
Hur, Manhoi
Irigoyen, Maria L.
Medina-Yerena, Diana
Nye, Danielle G.
Pérez Fons, Laura
Walling, Linda L.
author_facet Nye, Danielle G.
Irigoyen, Maria L.
Pérez Fons, Laura
Bohorquez-Chaux, Adriana
Hur, Manhoi
Medina-Yerena, Diana
Becerra-Lopez-Lavalle, Luis Augusto
Fraser, Paul D.
Walling, Linda L.
author_sort Nye, Danielle G.
collection Repository of Agricultural Research Outputs (CGSpace)
description Background Whiteflies are a global threat to crop yields, including the African subsistence crop cassava ( Manihot esculenta ). Outbreaks of superabundant whitefly populations throughout Eastern and Central Africa in recent years have dramatically increased the pressures of whitefly feeding and virus transmission on cassava. Whitefly-transmitted viral diseases threaten the food security of hundreds of millions of African farmers, highlighting the need for developing and deploying whitefly-resistant cassava. However, plant resistance to whiteflies remains largely poorly characterized at the genetic and molecular levels. Knowledge of cassava-defense programs also remains incomplete, limiting characterization of whitefly-resistance mechanisms. To better understand the genetic basis of whitefly resistance in cassava, we define the defense hormone- and Aleurotrachelus socialis (whitefly)-responsive transcriptome of whitefly-susceptible (COL2246) and whitefly-resistant (ECU72) cassava using RNA-seq. For broader comparison, hormone-responsive transcriptomes of Arabidopsis thaliana were also generated. Results Whitefly infestation, salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA) transcriptome responses of ECU72 and COL2246 were defined and analyzed. Strikingly, SA responses were largely reciprocal between the two cassava genotypes and we suggest candidate regulators. While susceptibility was associated with SA in COL2246, resistance to whitefly in ECU72 was associated with ABA, with SA-ABA antagonism observed. This was evidenced by expression of genes within the SA and ABA pathways and hormone levels during A. socialis infestation. Gene-enrichment analyses of whitefly- and hormone-responsive genes suggest the importance of fast-acting cell wall defenses (e.g., elicitor recognition, lignin biosynthesis) during early infestation stages in whitefly-resistant ECU72. A surge of ineffective immune and SA responses characterized the whitefly-susceptible COL2246’s response to late-stage nymphs. Lastly, in comparison with the model plant Arabidopsis, cassava’s hormone-responsive genes showed striking divergence in expression. Conclusions This study provides the first characterization of cassava’s global transcriptome responses to whitefly infestation and defense hormone treatment. Our analyses of ECU72 and COL2246 uncovered possible whitefly resistance/susceptibility mechanisms in cassava. Comparative analysis of cassava and Arabidopsis demonstrated that defense programs in Arabidopsis may not always mirror those in crop species. More broadly, our hormone-responsive transcriptomes will also provide a baseline for the cassava community to better understand global responses to other yield-limiting pests/pathogens.
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spelling CGSpace1384952025-11-11T19:02:00Z Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance Nye, Danielle G. Irigoyen, Maria L. Pérez Fons, Laura Bohorquez-Chaux, Adriana Hur, Manhoi Medina-Yerena, Diana Becerra-Lopez-Lavalle, Luis Augusto Fraser, Paul D. Walling, Linda L. pest control hormone atntagonists defense mechanisms Background Whiteflies are a global threat to crop yields, including the African subsistence crop cassava ( Manihot esculenta ). Outbreaks of superabundant whitefly populations throughout Eastern and Central Africa in recent years have dramatically increased the pressures of whitefly feeding and virus transmission on cassava. Whitefly-transmitted viral diseases threaten the food security of hundreds of millions of African farmers, highlighting the need for developing and deploying whitefly-resistant cassava. However, plant resistance to whiteflies remains largely poorly characterized at the genetic and molecular levels. Knowledge of cassava-defense programs also remains incomplete, limiting characterization of whitefly-resistance mechanisms. To better understand the genetic basis of whitefly resistance in cassava, we define the defense hormone- and Aleurotrachelus socialis (whitefly)-responsive transcriptome of whitefly-susceptible (COL2246) and whitefly-resistant (ECU72) cassava using RNA-seq. For broader comparison, hormone-responsive transcriptomes of Arabidopsis thaliana were also generated. Results Whitefly infestation, salicylic acid (SA), jasmonic acid (JA), ethylene (ET), and abscisic acid (ABA) transcriptome responses of ECU72 and COL2246 were defined and analyzed. Strikingly, SA responses were largely reciprocal between the two cassava genotypes and we suggest candidate regulators. While susceptibility was associated with SA in COL2246, resistance to whitefly in ECU72 was associated with ABA, with SA-ABA antagonism observed. This was evidenced by expression of genes within the SA and ABA pathways and hormone levels during A. socialis infestation. Gene-enrichment analyses of whitefly- and hormone-responsive genes suggest the importance of fast-acting cell wall defenses (e.g., elicitor recognition, lignin biosynthesis) during early infestation stages in whitefly-resistant ECU72. A surge of ineffective immune and SA responses characterized the whitefly-susceptible COL2246’s response to late-stage nymphs. Lastly, in comparison with the model plant Arabidopsis, cassava’s hormone-responsive genes showed striking divergence in expression. Conclusions This study provides the first characterization of cassava’s global transcriptome responses to whitefly infestation and defense hormone treatment. Our analyses of ECU72 and COL2246 uncovered possible whitefly resistance/susceptibility mechanisms in cassava. Comparative analysis of cassava and Arabidopsis demonstrated that defense programs in Arabidopsis may not always mirror those in crop species. More broadly, our hormone-responsive transcriptomes will also provide a baseline for the cassava community to better understand global responses to other yield-limiting pests/pathogens. 2023-12-20 2024-01-25T16:16:25Z 2024-01-25T16:16:25Z Journal Article https://hdl.handle.net/10568/138495 en Open Access application/pdf BioMed Central Nye, D.G.; Irigoyen, M.L.; Perez-Fons, L.; Bohorquez-Chaux, A.; Hur, M.; Medina-Yerena, D.; Becerra-Lopez-Lavalle, L.A.; Fraser, P.D.; Walling, L.L. (2023) Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance. BMC Plant Biology 23(1): ISSN: 1471-2229
spellingShingle pest control
hormone atntagonists
defense mechanisms
Nye, Danielle G.
Irigoyen, Maria L.
Pérez Fons, Laura
Bohorquez-Chaux, Adriana
Hur, Manhoi
Medina-Yerena, Diana
Becerra-Lopez-Lavalle, Luis Augusto
Fraser, Paul D.
Walling, Linda L.
Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title_full Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title_fullStr Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title_full_unstemmed Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title_short Integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
title_sort integrative transcriptomics reveals association of abscisic acid and lignin pathways with cassava whitefly resistance
topic pest control
hormone atntagonists
defense mechanisms
url https://hdl.handle.net/10568/138495
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