Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)

IntroductionReconstructive breeding based on autotetraploids to generate triploid varieties is a promising breeding strategy in banana (Musa spp.). Therefore understanding the molecular mechanisms underlying the phenotypic differences between the original diploid and its autopolyploid derivatives is...

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Main Authors: Ni Zhan, Li Li, Liping Zhang, Weidi He, Qiaosong Yang, Fangcheng Bi, Guiming Deng, Andrew Kiggundu, Ganjun Yi, Ou Sheng
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-01-01
Series:Frontiers in Sustainable Food Systems
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Online Access:https://www.frontiersin.org/articles/10.3389/fsufs.2022.1070108/full
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author Ni Zhan
Ni Zhan
Li Li
Li Li
Liping Zhang
Weidi He
Qiaosong Yang
Fangcheng Bi
Guiming Deng
Andrew Kiggundu
Ganjun Yi
Ou Sheng
author_facet Ni Zhan
Ni Zhan
Li Li
Li Li
Liping Zhang
Weidi He
Qiaosong Yang
Fangcheng Bi
Guiming Deng
Andrew Kiggundu
Ganjun Yi
Ou Sheng
author_sort Ni Zhan
collection DOAJ
description IntroductionReconstructive breeding based on autotetraploids to generate triploid varieties is a promising breeding strategy in banana (Musa spp.). Therefore understanding the molecular mechanisms underlying the phenotypic differences between the original diploid and its autopolyploid derivatives is of significant importance in such breeding programs of banana.MethodsIn this study, a number of non-chimeric autotetraploid plants, confirmed by flow cytometry and chromosome counting were obtained using colchicine treatment of ‘Pisang Berlin' (AA Group), a diploid banana cultivar highly resistant to Fusarium wilt Tropical Race 4 (Foc TR4) and widely cultivated in Asia.Results and discussionThe autotetraploids showed significant increase in plant height, pseudostem diameter, root length, leaf thickness, leaf area, and leaf chlorophyll content. Transcriptomic analysis indicated that differentially expressed genes were mainly enriched in plant hormone signal transduction, mitogen-activated protein kinase (MAPK) signaling pathway, and carbon fixation in photosynthetic organelles. The genes related to the metabolism, transport or signaling of auxin, abscisic acid (ABA), cytokinin (CTK) and gibberellin (GA), as well as the genes encoding essential enzymes in photosynthetic CO2 fixation were differentially expressed in leaves of autotetraploids and most of them were up-regulated. Metabolomic analysis revealed that the differentially accumulated metabolites were mainly involved in plant hormone signal transduction, porphyrin and chlorophyll metabolism, indole alkaloid biosynthesis, and carbon fixation in photosynthetic organelles. The results therefore, demonstrate that the hormones IAA, ABA, and photosynthetic regulation may play a vital role in the observed enhancement in the autotetraploids. These could be used as molecular and biochemical markers to facilitate the generation of triploid progenies as suitable new varieties for cultivation.
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spelling doaj.art-038d356e3a764c65b7edadb26b9614e72023-01-04T16:51:53ZengFrontiers Media S.A.Frontiers in Sustainable Food Systems2571-581X2023-01-01610.3389/fsufs.2022.10701081070108Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)Ni Zhan0Ni Zhan1Li Li2Li Li3Liping Zhang4Weidi He5Qiaosong Yang6Fangcheng Bi7Guiming Deng8Andrew Kiggundu9Ganjun Yi10Ou Sheng11Key Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaCollege of Life Science, Langfang Normal University, Langfang, Hebei, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of Horticultural Plant Biology, Ministry of Education, College of Horticulture and Forestry, Huazhong Agricultural University, Wuhan, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaGenomics Applications Platform, National Agricultural Research Organisation (NARO), Entebbe, UgandaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaKey Laboratory of South Subtropical Fruit Biology and Genetic Resource Utilization, Guangdong Provincial Key Laboratory of Tropical and Subtropical Fruit Tree Research, Institute of Fruit Tree Research, Guangdong Academy of Agricultural Sciences, Ministry of Agriculture and Rural Affairs, Guangzhou, ChinaIntroductionReconstructive breeding based on autotetraploids to generate triploid varieties is a promising breeding strategy in banana (Musa spp.). Therefore understanding the molecular mechanisms underlying the phenotypic differences between the original diploid and its autopolyploid derivatives is of significant importance in such breeding programs of banana.MethodsIn this study, a number of non-chimeric autotetraploid plants, confirmed by flow cytometry and chromosome counting were obtained using colchicine treatment of ‘Pisang Berlin' (AA Group), a diploid banana cultivar highly resistant to Fusarium wilt Tropical Race 4 (Foc TR4) and widely cultivated in Asia.Results and discussionThe autotetraploids showed significant increase in plant height, pseudostem diameter, root length, leaf thickness, leaf area, and leaf chlorophyll content. Transcriptomic analysis indicated that differentially expressed genes were mainly enriched in plant hormone signal transduction, mitogen-activated protein kinase (MAPK) signaling pathway, and carbon fixation in photosynthetic organelles. The genes related to the metabolism, transport or signaling of auxin, abscisic acid (ABA), cytokinin (CTK) and gibberellin (GA), as well as the genes encoding essential enzymes in photosynthetic CO2 fixation were differentially expressed in leaves of autotetraploids and most of them were up-regulated. Metabolomic analysis revealed that the differentially accumulated metabolites were mainly involved in plant hormone signal transduction, porphyrin and chlorophyll metabolism, indole alkaloid biosynthesis, and carbon fixation in photosynthetic organelles. The results therefore, demonstrate that the hormones IAA, ABA, and photosynthetic regulation may play a vital role in the observed enhancement in the autotetraploids. These could be used as molecular and biochemical markers to facilitate the generation of triploid progenies as suitable new varieties for cultivation.https://www.frontiersin.org/articles/10.3389/fsufs.2022.1070108/fullautotetraploiddiploidhormonal regulationtranscriptomemetabolomecolchicine
spellingShingle Ni Zhan
Ni Zhan
Li Li
Li Li
Liping Zhang
Weidi He
Qiaosong Yang
Fangcheng Bi
Guiming Deng
Andrew Kiggundu
Ganjun Yi
Ou Sheng
Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
Frontiers in Sustainable Food Systems
autotetraploid
diploid
hormonal regulation
transcriptome
metabolome
colchicine
title Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
title_full Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
title_fullStr Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
title_full_unstemmed Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
title_short Transcriptome and metabolome profiling provide insights into hormone-mediated enhanced growth in autotetraploid seedlings of banana (Musa spp.)
title_sort transcriptome and metabolome profiling provide insights into hormone mediated enhanced growth in autotetraploid seedlings of banana musa spp
topic autotetraploid
diploid
hormonal regulation
transcriptome
metabolome
colchicine
url https://www.frontiersin.org/articles/10.3389/fsufs.2022.1070108/full
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