Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis
Abstract Background Yellow lupine (Lupinus luteus L.) is a high-protein crop of considerable economic and ecological significance. It has the ability to fix atmospheric nitrogen in symbiosis with Rhizobium, enriching marginal soils with this essential nutrient and reducing the need for artificial fe...
Saved in:
| Main Authors: | , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2024-11-01
|
| Series: | BMC Plant Biology |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12870-024-05748-4 |
| Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
| _version_ | 1846172112269606912 |
|---|---|
| author | Sebastian Burchardt Małgorzata Czernicka Agata Kućko Wojciech Pokora Małgorzata Kapusta Krzysztof Domagalski Katarzyna Jasieniecka-Gazarkiewicz Jacek Karwaszewski Emilia Wilmowicz |
| author_facet | Sebastian Burchardt Małgorzata Czernicka Agata Kućko Wojciech Pokora Małgorzata Kapusta Krzysztof Domagalski Katarzyna Jasieniecka-Gazarkiewicz Jacek Karwaszewski Emilia Wilmowicz |
| author_sort | Sebastian Burchardt |
| collection | DOAJ |
| description | Abstract Background Yellow lupine (Lupinus luteus L.) is a high-protein crop of considerable economic and ecological significance. It has the ability to fix atmospheric nitrogen in symbiosis with Rhizobium, enriching marginal soils with this essential nutrient and reducing the need for artificial fertilizers. Additionally, lupine produces seeds with a high protein content, making it valuable for animal feed production. However, drought negatively affects lupine development, its mutualistic relationship with bacteria, and overall yield. To understand how lupine responds to this stress, global transcriptome sequencing was conducted, along with in-depth biochemical, chromatography, and microscopy analyses of roots subjected to drought. The results presented here contribute to strategies aimed at mitigating the effects of water deficit on lupine growth and development. Results Based on RNA-seq, drought-specific genes were identified and annotated to biological pathways involved in phytohormone biosynthesis/signaling, lipid metabolism, and redox homeostasis. Our findings indicate that drought-induced disruption of redox balance characterized by the upregulation of reactive oxygen species (ROS) scavenging enzymes, coincided with the accumulation of lipid-metabolizing enzymes, such as phospholipase D (PLD) and lipoxygenase (LOX). This disruption also led to modifications in lipid homeostasis, including increased levels of triacylglycerols (TAG) and free fatty acids (FFA), along with a decrease in polar lipid content. Additionally, the stress response involved alterations in the transcriptional regulation of the linolenic acid metabolism network, resulting in changes in the composition of fatty acids containing 18 carbons. Conclusion The first comprehensive global transcriptomic profiles of lupine roots, combined with the identification of key stress-responsive molecules, represent a significant advancement in understanding lupine’s responses to abiotic stress. The increased expression of the Δ12DESATURASE gene and enhanced PLD activity lead to higher level of linoleic acid (18:2), which is subsequently oxidized by LOX, resulting in membrane damage and malondialdehyde (MDA) accumulation. Oxidative stress elevates the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT), while the conversion of FFAs into TAGs provides protection against ROS. This research offers valuable molecular and biochemical candidates with significant potential to enhance drought tolerance . It enables innovative strategies in lupine breeding and crop improvement to address critical agricultural challenges. |
| format | Article |
| id | doaj-art-8f017365daa44bb28f68f970a44fb92b |
| institution | Kabale University |
| issn | 1471-2229 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj-art-8f017365daa44bb28f68f970a44fb92b2024-11-10T12:15:12ZengBMCBMC Plant Biology1471-22292024-11-0124112010.1186/s12870-024-05748-4Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasisSebastian Burchardt0Małgorzata Czernicka1Agata Kućko2Wojciech Pokora3Małgorzata Kapusta4Krzysztof Domagalski5Katarzyna Jasieniecka-Gazarkiewicz6Jacek Karwaszewski7Emilia Wilmowicz8Chair of Plant Physiology and Biotechnology, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus UniversityDepartment of Plant Biology and Biotechnology, Faculty of Biotechnology and Horticulture, University of Agriculture in KrakowDepartment of Plant Physiology, Institute of Biology, Warsaw University of Life Sciences- SGGWDepartment of Plant Physiology and Biotechnology, University of GdańskBioimaging Laboratory, University of GdańskDepartment of Immunology, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus UniversityIntercollegiate Faculty of Biotechnology, University of Gdansk and Medical University of GdańskChair of Plant Physiology and Biotechnology, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus UniversityChair of Plant Physiology and Biotechnology, Faculty of Biological and Veterinary Sciences, Nicolaus Copernicus UniversityAbstract Background Yellow lupine (Lupinus luteus L.) is a high-protein crop of considerable economic and ecological significance. It has the ability to fix atmospheric nitrogen in symbiosis with Rhizobium, enriching marginal soils with this essential nutrient and reducing the need for artificial fertilizers. Additionally, lupine produces seeds with a high protein content, making it valuable for animal feed production. However, drought negatively affects lupine development, its mutualistic relationship with bacteria, and overall yield. To understand how lupine responds to this stress, global transcriptome sequencing was conducted, along with in-depth biochemical, chromatography, and microscopy analyses of roots subjected to drought. The results presented here contribute to strategies aimed at mitigating the effects of water deficit on lupine growth and development. Results Based on RNA-seq, drought-specific genes were identified and annotated to biological pathways involved in phytohormone biosynthesis/signaling, lipid metabolism, and redox homeostasis. Our findings indicate that drought-induced disruption of redox balance characterized by the upregulation of reactive oxygen species (ROS) scavenging enzymes, coincided with the accumulation of lipid-metabolizing enzymes, such as phospholipase D (PLD) and lipoxygenase (LOX). This disruption also led to modifications in lipid homeostasis, including increased levels of triacylglycerols (TAG) and free fatty acids (FFA), along with a decrease in polar lipid content. Additionally, the stress response involved alterations in the transcriptional regulation of the linolenic acid metabolism network, resulting in changes in the composition of fatty acids containing 18 carbons. Conclusion The first comprehensive global transcriptomic profiles of lupine roots, combined with the identification of key stress-responsive molecules, represent a significant advancement in understanding lupine’s responses to abiotic stress. The increased expression of the Δ12DESATURASE gene and enhanced PLD activity lead to higher level of linoleic acid (18:2), which is subsequently oxidized by LOX, resulting in membrane damage and malondialdehyde (MDA) accumulation. Oxidative stress elevates the activities of superoxide dismutase (SOD), ascorbate peroxidase (APX), and catalase (CAT), while the conversion of FFAs into TAGs provides protection against ROS. This research offers valuable molecular and biochemical candidates with significant potential to enhance drought tolerance . It enables innovative strategies in lupine breeding and crop improvement to address critical agricultural challenges.https://doi.org/10.1186/s12870-024-05748-4LipoxygenaseNGSPhospholipase DPhytohormonesRedox balanceRNA-seq |
| spellingShingle | Sebastian Burchardt Małgorzata Czernicka Agata Kućko Wojciech Pokora Małgorzata Kapusta Krzysztof Domagalski Katarzyna Jasieniecka-Gazarkiewicz Jacek Karwaszewski Emilia Wilmowicz Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis BMC Plant Biology Lipoxygenase NGS Phospholipase D Phytohormones Redox balance RNA-seq |
| title | Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis |
| title_full | Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis |
| title_fullStr | Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis |
| title_full_unstemmed | Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis |
| title_short | Exploring the response of yellow lupine (Lupinus luteus L.) root to drought mediated by pathways related to phytohormones, lipid, and redox homeostasis |
| title_sort | exploring the response of yellow lupine lupinus luteus l root to drought mediated by pathways related to phytohormones lipid and redox homeostasis |
| topic | Lipoxygenase NGS Phospholipase D Phytohormones Redox balance RNA-seq |
| url | https://doi.org/10.1186/s12870-024-05748-4 |
| work_keys_str_mv | AT sebastianburchardt exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT małgorzataczernicka exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT agatakucko exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT wojciechpokora exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT małgorzatakapusta exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT krzysztofdomagalski exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT katarzynajasienieckagazarkiewicz exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT jacekkarwaszewski exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis AT emiliawilmowicz exploringtheresponseofyellowlupinelupinusluteuslroottodroughtmediatedbypathwaysrelatedtophytohormoneslipidandredoxhomeostasis |