Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes

Abstract Chickpea, a vital legume crop, is highly susceptible to cold stress, especially during its reproductive phase, resulting in significant flower and pod abortions and reduced seed yield. Our previous study demonstrated that cold acclimation is effective in enhancing cold tolerance but benefit...

Full description

Saved in:
Bibliographic Details
Main Authors: Deeksha Padhiar, Sarbjeet Kaur, Anju Rani, Uday Chand Jha, P. V. Vara Prasad, Kamal Dev Sharma, Sanjeev Kumar, Swarup Kumar Parida, Kadambot H. M. Siddique, Harsh Nayyar
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Scientific Reports
Subjects:
Online Access:https://doi.org/10.1038/s41598-025-03211-4
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850136605942087680
author Deeksha Padhiar
Sarbjeet Kaur
Anju Rani
Uday Chand Jha
P. V. Vara Prasad
Kamal Dev Sharma
Sanjeev Kumar
Swarup Kumar Parida
Kadambot H. M. Siddique
Harsh Nayyar
author_facet Deeksha Padhiar
Sarbjeet Kaur
Anju Rani
Uday Chand Jha
P. V. Vara Prasad
Kamal Dev Sharma
Sanjeev Kumar
Swarup Kumar Parida
Kadambot H. M. Siddique
Harsh Nayyar
author_sort Deeksha Padhiar
collection DOAJ
description Abstract Chickpea, a vital legume crop, is highly susceptible to cold stress, especially during its reproductive phase, resulting in significant flower and pod abortions and reduced seed yield. Our previous study demonstrated that cold acclimation is effective in enhancing cold tolerance but benefits only cold-tolerant (CT) genotypes, while cold-sensitive (CS) genotypes remain unaffected. In this extended study aimed at probing the detailed mechanisms of this differential response, we further examined the expression profiles of enzymes involved in the synthesis and breakdown of osmolytes (pyrroline-5-carboxylate synthase, proline dehydrogenase (PDH), betaine aldehyde dehydrogenase) and sugars (sucrose synthase, acid invertase, trehalose-6-phosphate synthase, trehalose-6-phosphate phosphatase, and trehalase activity), along with the expression of various antioxidants (superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase) in both CT and CS genotypes. Seeds of two contrasting chickpea genotypes, cold-tolerant ICC 17258 and cold-sensitive ICC 15567, were planted in pots during the first week of November in an outdoor field environment. After 40 days, the plants were transferred to walk-in growth chambers for cold acclimation at specific temperatures. Initially, the plants were exposed the plants to 25/18℃ (pre-acclimation stage; PAS) for 2 days, followed by a 21-day cold acclimation period with progressively decreasing temperatures over seven days for each cold acclimation stage (CAS): CAS1 (21/13℃), CAS2 (18/10℃), and CAS3 (15/8℃). Subsequently, the plants were subjected to cold stress at 13/7℃ for 15 days and then exposed to 30/23℃ (12 h day/night) until maturity. Our findings demonstrated that the expression of various enzymes involved in the synthesis of osmolytes and sugars in leaves, anthers, and ovules was significantly upregulated during the cold acclimation process in the CT chickpea genotypes but not in the CS genotypes. This enhanced metabolic activity, coupled with elevated levels of enzymatic antioxidants during the acclimation process, contributed to improved leaf water status, photosynthetic efficiency, and ultimately, superior reproductive performance (pollen germination, pollen viability, stigma receptivity, and ovule viability) under cold stress conditions compared to CS genotypes. The enhanced cold tolerance observed in the CT genotypes is likely attributable to their genetic predisposition and efficient stress defense mechanisms facilitated by the upregulated expression of cold-responsive enzymes.
format Article
id doaj-art-fee41a1d7d3f4b4d8c9a5a77c28598d7
institution OA Journals
issn 2045-2322
language English
publishDate 2025-06-01
publisher Nature Portfolio
record_format Article
series Scientific Reports
spelling doaj-art-fee41a1d7d3f4b4d8c9a5a77c28598d72025-08-20T02:31:04ZengNature PortfolioScientific Reports2045-23222025-06-0115112110.1038/s41598-025-03211-4Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypesDeeksha Padhiar0Sarbjeet Kaur1Anju Rani2Uday Chand Jha3P. V. Vara Prasad4Kamal Dev Sharma5Sanjeev Kumar6Swarup Kumar Parida7Kadambot H. M. Siddique8Harsh Nayyar9Department of Botany, Panjab UniversityDepartment of Botany, Panjab UniversityDepartment of Botany, Panjab UniversityCrop Improvement Division, Indian Institute of Pulses ResearchDepartment of Agronomy, Kansas State UniversityDepartment of Agriculture Biotechnology, CSK Himachal Pradesh Agricultural UniversityDepartment of Plant Sciences, Central University of PunjabNational Institute of Plant Genome ResearchThe UWA Institute of Agriculture, The University of Western AustraliaDepartment of Botany, Panjab UniversityAbstract Chickpea, a vital legume crop, is highly susceptible to cold stress, especially during its reproductive phase, resulting in significant flower and pod abortions and reduced seed yield. Our previous study demonstrated that cold acclimation is effective in enhancing cold tolerance but benefits only cold-tolerant (CT) genotypes, while cold-sensitive (CS) genotypes remain unaffected. In this extended study aimed at probing the detailed mechanisms of this differential response, we further examined the expression profiles of enzymes involved in the synthesis and breakdown of osmolytes (pyrroline-5-carboxylate synthase, proline dehydrogenase (PDH), betaine aldehyde dehydrogenase) and sugars (sucrose synthase, acid invertase, trehalose-6-phosphate synthase, trehalose-6-phosphate phosphatase, and trehalase activity), along with the expression of various antioxidants (superoxide dismutase, catalase, ascorbate peroxidase, and glutathione reductase) in both CT and CS genotypes. Seeds of two contrasting chickpea genotypes, cold-tolerant ICC 17258 and cold-sensitive ICC 15567, were planted in pots during the first week of November in an outdoor field environment. After 40 days, the plants were transferred to walk-in growth chambers for cold acclimation at specific temperatures. Initially, the plants were exposed the plants to 25/18℃ (pre-acclimation stage; PAS) for 2 days, followed by a 21-day cold acclimation period with progressively decreasing temperatures over seven days for each cold acclimation stage (CAS): CAS1 (21/13℃), CAS2 (18/10℃), and CAS3 (15/8℃). Subsequently, the plants were subjected to cold stress at 13/7℃ for 15 days and then exposed to 30/23℃ (12 h day/night) until maturity. Our findings demonstrated that the expression of various enzymes involved in the synthesis of osmolytes and sugars in leaves, anthers, and ovules was significantly upregulated during the cold acclimation process in the CT chickpea genotypes but not in the CS genotypes. This enhanced metabolic activity, coupled with elevated levels of enzymatic antioxidants during the acclimation process, contributed to improved leaf water status, photosynthetic efficiency, and ultimately, superior reproductive performance (pollen germination, pollen viability, stigma receptivity, and ovule viability) under cold stress conditions compared to CS genotypes. The enhanced cold tolerance observed in the CT genotypes is likely attributable to their genetic predisposition and efficient stress defense mechanisms facilitated by the upregulated expression of cold-responsive enzymes.https://doi.org/10.1038/s41598-025-03211-4ChickpeaChilling; stressProlineSugar dynamicsOsmolytesAntioxidant metabolism
spellingShingle Deeksha Padhiar
Sarbjeet Kaur
Anju Rani
Uday Chand Jha
P. V. Vara Prasad
Kamal Dev Sharma
Sanjeev Kumar
Swarup Kumar Parida
Kadambot H. M. Siddique
Harsh Nayyar
Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
Scientific Reports
Chickpea
Chilling; stress
Proline
Sugar dynamics
Osmolytes
Antioxidant metabolism
title Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
title_full Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
title_fullStr Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
title_full_unstemmed Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
title_short Deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
title_sort deciphering the dynamics of enzymes associated with the synthesis of cryoprotectants during cold acclimation in contrasting chickpea genotypes
topic Chickpea
Chilling; stress
Proline
Sugar dynamics
Osmolytes
Antioxidant metabolism
url https://doi.org/10.1038/s41598-025-03211-4
work_keys_str_mv AT deekshapadhiar decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT sarbjeetkaur decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT anjurani decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT udaychandjha decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT pvvaraprasad decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT kamaldevsharma decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT sanjeevkumar decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT swarupkumarparida decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT kadambothmsiddique decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes
AT harshnayyar decipheringthedynamicsofenzymesassociatedwiththesynthesisofcryoprotectantsduringcoldacclimationincontrastingchickpeagenotypes