Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves

Polyamines have been implicated in ameliorating the detrimental effects of drought and saline conditions on plant growth and development. The independent impact of these two abiotic stresses on polyamine (PA) biosynthesis, catabolism, and homeostasis, as well as on their transcript abundance in toma...

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Main Authors: Rakesh K. Upadhyay, Tahira Fatima, Avtar K. Handa, Autar K. Mattoo
Format: Article
Language:English
Published: Frontiers Media S.A. 2021-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2021.743568/full
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author Rakesh K. Upadhyay
Rakesh K. Upadhyay
Tahira Fatima
Avtar K. Handa
Autar K. Mattoo
author_facet Rakesh K. Upadhyay
Rakesh K. Upadhyay
Tahira Fatima
Avtar K. Handa
Autar K. Mattoo
author_sort Rakesh K. Upadhyay
collection DOAJ
description Polyamines have been implicated in ameliorating the detrimental effects of drought and saline conditions on plant growth and development. The independent impact of these two abiotic stresses on polyamine (PA) biosynthesis, catabolism, and homeostasis, as well as on their transcript abundance in tomato leaves, is presented here. We show that the total levels of putrescine (PUT), spermidine (SPD), and spermine (SPM) increase up to 72 h during drought and up to 48 h during salinity stress before their precipitable drop thereafter. Thus, tomato plants maintain survivability to drought as well as salinity stress for up to 3 and 2 days, respectively. Independent multivariant analyses of drought and salinity stress kinetic data separately showed a closer association with levels of free, conjugated, and bound forms of SPD and SPM, but not with free or bound PUT. However, combined multivariant analyses showed a closer association of free SPD, conjugated SPD, and bound SPD with both stresses; SPD-bound and SPM conjugated with drought; and free SPM and conjugated PUT with salinity stress, respectively. PA biosynthesis genes, ARG1, SPDS1, and SAMDc3, segregated with drought and SPDS2 with salinity stress. PA catabolic genes CuAO4-like and PAO4 were associated with drought and salinity stresses, respectively, suggesting differential involvement of PA biosynthesis and catabolic genes in drought and salinity stresses. Pearson correlation indicated mostly positive correlations between the levels of free, conjugated, and bound forms of PUT, SPD, and SPM under drought and salinity stress. However, negative correlations were mostly seen between the levels of various forms of the PAs and their biosynthesis/catabolic genes. Levels of different PA forms had a twofold higher negative correlation during drought as compared to salinity stress (66 vs. 32) and with transcript levels of PA biosynthesis and catabolic genes. Transcripts of light-harvesting chlorophyll a/b-binding genes were generally positively associated with different forms of PAs but negatively to carbon flow genes. Most of the PA biosynthesis genes were coordinately regulated under both stresses. Collectively, these results indicate that PAs are distinctly regulated under drought and salinity stress with different but specific homologs of PA biosynthesis and catabolic genes contributing to the accumulation of free, conjugated, and bound forms of PAs.
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spelling doaj.art-859cae7e2a37450f99676eabd82644a22022-12-21T22:41:10ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2021-10-011210.3389/fpls.2021.743568743568Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) LeavesRakesh K. Upadhyay0Rakesh K. Upadhyay1Tahira Fatima2Avtar K. Handa3Autar K. Mattoo4Sustainable Agricultural Systems Laboratory, Henry A. Wallace Beltsville Agricultural Research Center, United States Department of Agriculture-Agricultural Research Service, Beltsville, MD, United StatesCenter of Plant Biology, Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesCenter of Plant Biology, Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesCenter of Plant Biology, Department of Horticulture and Landscape Architecture, Purdue University, West Lafayette, IN, United StatesSustainable Agricultural Systems Laboratory, Henry A. Wallace Beltsville Agricultural Research Center, United States Department of Agriculture-Agricultural Research Service, Beltsville, MD, United StatesPolyamines have been implicated in ameliorating the detrimental effects of drought and saline conditions on plant growth and development. The independent impact of these two abiotic stresses on polyamine (PA) biosynthesis, catabolism, and homeostasis, as well as on their transcript abundance in tomato leaves, is presented here. We show that the total levels of putrescine (PUT), spermidine (SPD), and spermine (SPM) increase up to 72 h during drought and up to 48 h during salinity stress before their precipitable drop thereafter. Thus, tomato plants maintain survivability to drought as well as salinity stress for up to 3 and 2 days, respectively. Independent multivariant analyses of drought and salinity stress kinetic data separately showed a closer association with levels of free, conjugated, and bound forms of SPD and SPM, but not with free or bound PUT. However, combined multivariant analyses showed a closer association of free SPD, conjugated SPD, and bound SPD with both stresses; SPD-bound and SPM conjugated with drought; and free SPM and conjugated PUT with salinity stress, respectively. PA biosynthesis genes, ARG1, SPDS1, and SAMDc3, segregated with drought and SPDS2 with salinity stress. PA catabolic genes CuAO4-like and PAO4 were associated with drought and salinity stresses, respectively, suggesting differential involvement of PA biosynthesis and catabolic genes in drought and salinity stresses. Pearson correlation indicated mostly positive correlations between the levels of free, conjugated, and bound forms of PUT, SPD, and SPM under drought and salinity stress. However, negative correlations were mostly seen between the levels of various forms of the PAs and their biosynthesis/catabolic genes. Levels of different PA forms had a twofold higher negative correlation during drought as compared to salinity stress (66 vs. 32) and with transcript levels of PA biosynthesis and catabolic genes. Transcripts of light-harvesting chlorophyll a/b-binding genes were generally positively associated with different forms of PAs but negatively to carbon flow genes. Most of the PA biosynthesis genes were coordinately regulated under both stresses. Collectively, these results indicate that PAs are distinctly regulated under drought and salinity stress with different but specific homologs of PA biosynthesis and catabolic genes contributing to the accumulation of free, conjugated, and bound forms of PAs.https://www.frontiersin.org/articles/10.3389/fpls.2021.743568/fullpolyamineputrescine (PUT)spermidine (SPD)spermine (SPM)tomatodrought
spellingShingle Rakesh K. Upadhyay
Rakesh K. Upadhyay
Tahira Fatima
Avtar K. Handa
Autar K. Mattoo
Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
Frontiers in Plant Science
polyamine
putrescine (PUT)
spermidine (SPD)
spermine (SPM)
tomato
drought
title Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
title_full Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
title_fullStr Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
title_full_unstemmed Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
title_short Differential Association of Free, Conjugated, and Bound Forms of Polyamines and Transcript Abundance of Their Biosynthetic and Catabolic Genes During Drought/Salinity Stress in Tomato (Solanum lycopersicum L.) Leaves
title_sort differential association of free conjugated and bound forms of polyamines and transcript abundance of their biosynthetic and catabolic genes during drought salinity stress in tomato solanum lycopersicum l leaves
topic polyamine
putrescine (PUT)
spermidine (SPD)
spermine (SPM)
tomato
drought
url https://www.frontiersin.org/articles/10.3389/fpls.2021.743568/full
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