The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas
Tomato (Solanum lycopersicum) is a model species for studying fruit development, wounding, herbivory, and pathogen attack. Despite tomato’s world-wide economic importance and the role of chloroplasts as metabolic hubs and integrators of environmental cues, little is known about the stromal proteome...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fpls.2023.1020275/full |
| _version_ | 1797735977672769536 |
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| author | Oindrila Bhattacharya Irma Ortiz Nathan Hendricks Linda L. Walling Linda L. Walling |
| author_facet | Oindrila Bhattacharya Irma Ortiz Nathan Hendricks Linda L. Walling Linda L. Walling |
| author_sort | Oindrila Bhattacharya |
| collection | DOAJ |
| description | Tomato (Solanum lycopersicum) is a model species for studying fruit development, wounding, herbivory, and pathogen attack. Despite tomato’s world-wide economic importance and the role of chloroplasts as metabolic hubs and integrators of environmental cues, little is known about the stromal proteome of tomato. Using a high-yielding protocol for chloroplast and stromal protein isolation, MudPIT nano-LC-MS/MS analyses, a robust in-house protein database (the Atlas) for predicting the plastid localization of tomato proteins, and rigorous selection criteria for inclusion/exclusion in the stromal proteome, we identified 1,278 proteins of the tomato stromal proteome. We provide one of the most robust stromal proteomes available to date with empirical evidence for 545 and 92 proteins not previously described for tomato plastids and the Arabidopsis stroma, respectively. The relative abundance of tomato stromal proteins was determined using the exponentially modified protein abundance index (emPAI). Comparison of the abundance of tomato and Arabidopsis stromal proteomes provided evidence for the species-specific nature of stromal protein homeostasis. The manual curation of the tomato stromal proteome classified proteins into ten functional categories resulting in an accessible compendium of tomato chloroplast proteins. After curation, only 91 proteins remained as unknown, uncharacterized or as enzymes with unknown functions. The curation of the tomato stromal proteins also indicated that tomato has a number of paralogous proteins, not present in Arabidopsis, which accumulated to different levels in chloroplasts. As some of these proteins function in key metabolic pathways or in perceiving or transmitting signals critical for plant adaptation to biotic and abiotic stress, these data suggest that tomato may modulate the bidirectional communication between chloroplasts and nuclei in a novel manner. The stromal proteome provides a fertile ground for future mechanistic studies in the field of tomato chloroplast-nuclear signaling and are foundational for our goal of elucidating the dynamics of the stromal proteome controlled by the solanaceous-specific, stromal, and wound-inducible leucine aminopeptidase A of tomato. |
| first_indexed | 2024-03-12T13:06:54Z |
| format | Article |
| id | doaj.art-f57e846d9c8a420db21fc07e4e2b9444 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-03-12T13:06:54Z |
| publishDate | 2023-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-f57e846d9c8a420db21fc07e4e2b94442023-08-28T14:43:40ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-08-011410.3389/fpls.2023.10202751020275The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction AtlasOindrila Bhattacharya0Irma Ortiz1Nathan Hendricks2Linda L. Walling3Linda L. Walling4Department of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United StatesDepartment of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United StatesInstitute of Integrative Genome Biology, University of California, Riverside, Riverside, CA, United StatesDepartment of Botany and Plant Sciences, University of California, Riverside, Riverside, CA, United StatesInstitute of Integrative Genome Biology, University of California, Riverside, Riverside, CA, United StatesTomato (Solanum lycopersicum) is a model species for studying fruit development, wounding, herbivory, and pathogen attack. Despite tomato’s world-wide economic importance and the role of chloroplasts as metabolic hubs and integrators of environmental cues, little is known about the stromal proteome of tomato. Using a high-yielding protocol for chloroplast and stromal protein isolation, MudPIT nano-LC-MS/MS analyses, a robust in-house protein database (the Atlas) for predicting the plastid localization of tomato proteins, and rigorous selection criteria for inclusion/exclusion in the stromal proteome, we identified 1,278 proteins of the tomato stromal proteome. We provide one of the most robust stromal proteomes available to date with empirical evidence for 545 and 92 proteins not previously described for tomato plastids and the Arabidopsis stroma, respectively. The relative abundance of tomato stromal proteins was determined using the exponentially modified protein abundance index (emPAI). Comparison of the abundance of tomato and Arabidopsis stromal proteomes provided evidence for the species-specific nature of stromal protein homeostasis. The manual curation of the tomato stromal proteome classified proteins into ten functional categories resulting in an accessible compendium of tomato chloroplast proteins. After curation, only 91 proteins remained as unknown, uncharacterized or as enzymes with unknown functions. The curation of the tomato stromal proteins also indicated that tomato has a number of paralogous proteins, not present in Arabidopsis, which accumulated to different levels in chloroplasts. As some of these proteins function in key metabolic pathways or in perceiving or transmitting signals critical for plant adaptation to biotic and abiotic stress, these data suggest that tomato may modulate the bidirectional communication between chloroplasts and nuclei in a novel manner. The stromal proteome provides a fertile ground for future mechanistic studies in the field of tomato chloroplast-nuclear signaling and are foundational for our goal of elucidating the dynamics of the stromal proteome controlled by the solanaceous-specific, stromal, and wound-inducible leucine aminopeptidase A of tomato.https://www.frontiersin.org/articles/10.3389/fpls.2023.1020275/fullchloroplastleucine aminopeptidaselumenal proteinsstromaredoxprotein homeostasis |
| spellingShingle | Oindrila Bhattacharya Irma Ortiz Nathan Hendricks Linda L. Walling Linda L. Walling The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas Frontiers in Plant Science chloroplast leucine aminopeptidase lumenal proteins stroma redox protein homeostasis |
| title | The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas |
| title_full | The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas |
| title_fullStr | The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas |
| title_full_unstemmed | The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas |
| title_short | The tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein-localization prediction Atlas |
| title_sort | tomato chloroplast stromal proteome compendium elucidated by leveraging a plastid protein localization prediction atlas |
| topic | chloroplast leucine aminopeptidase lumenal proteins stroma redox protein homeostasis |
| url | https://www.frontiersin.org/articles/10.3389/fpls.2023.1020275/full |
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