The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense

Grain amaranths tolerate stress and produce highly nutritious seeds. We have identified several (a)biotic stress-responsive genes of unknown function in Amaranthus hypochondriacus, including the so-called Ah24 gene. Ah24 was expressed in young or developing tissues; it was also strongly induced by m...

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Main Authors: Julio Armando Massange-Sanchez, Paola Andrea Palmeros-Suarez, Norma Angelica Martinez-Gallardo, Paula Andrea Castrillon-Arbelaez, Hamlet eAviles-Arnaut, Fulgencio eAlatorre-Cobo, Axel eTiessen, John Paul Délano-Frier
Format: Article
Language:English
Published: Frontiers Media S.A. 2015-08-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2015.00602/full
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author Julio Armando Massange-Sanchez
Paola Andrea Palmeros-Suarez
Norma Angelica Martinez-Gallardo
Paula Andrea Castrillon-Arbelaez
Hamlet eAviles-Arnaut
Fulgencio eAlatorre-Cobo
Axel eTiessen
John Paul Délano-Frier
author_facet Julio Armando Massange-Sanchez
Paola Andrea Palmeros-Suarez
Norma Angelica Martinez-Gallardo
Paula Andrea Castrillon-Arbelaez
Hamlet eAviles-Arnaut
Fulgencio eAlatorre-Cobo
Axel eTiessen
John Paul Délano-Frier
author_sort Julio Armando Massange-Sanchez
collection DOAJ
description Grain amaranths tolerate stress and produce highly nutritious seeds. We have identified several (a)biotic stress-responsive genes of unknown function in Amaranthus hypochondriacus, including the so-called Ah24 gene. Ah24 was expressed in young or developing tissues; it was also strongly induced by mechanical damage, insect herbivory and methyl jasmonate and in meristems and newly emerging leaves of severely defoliated plants. Interestingly, an in silico analysis of its 1304 bp promoter region showed a predominance of regulatory boxes involved in development, but not in defense. The Ah24 cDNA encodes a predicted cytosolic protein of 164 amino acids, the localization of which was confirmed by confocal microscopy. Additional in silico analysis identified several other Ah24 homologs, present almost exclusively in plants belonging to the Caryophyllales. The possible function of this gene in planta was examined in transgenic Ah24 overexpressing Arabidopsis thaliana and Nicotiana tabacum plants. Transformed Arabidopsis showed enhanced vegetative growth and increased leaf number with no penalty in one fitness component, such as seed yield, in experimental conditions. Transgenic tobacco plants, which grew and reproduced normally, had increased insect herbivory resistance. Modified vegetative growth in transgenic Arabidopsis coincided with significant changes in the expression of genes controlling phytohormone synthesis or signaling, whereas increased resistance to insect herbivory in transgenic tobacco coincided with higher jasmonic acid and proteinase inhibitor activity levels, plus the accumulation of nicotine and several other putative defense-related metabolites. It is proposed that the primary role of the Ah24 gene in A. hypochondriacus is to contribute to a rapid recovery post-wounding or defoliation, although its participation in defense against insect herbivory is also plausible.
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spelling doaj.art-78af5fba7b4a4975bddbbdf654f1f8a32022-12-21T20:01:04ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2015-08-01610.3389/fpls.2015.00602145505The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defenseJulio Armando Massange-Sanchez0Paola Andrea Palmeros-Suarez1Norma Angelica Martinez-Gallardo2Paula Andrea Castrillon-Arbelaez3Hamlet eAviles-Arnaut4Fulgencio eAlatorre-Cobo5Axel eTiessen6John Paul Délano-Frier7Centro de Investigación y de Estudios Avanzados del I.P.N., Unidad IrapuatoCentro de Investigación y de Estudios Avanzados del I.P.N., Unidad IrapuatoCentro de Investigación y de Estudios Avanzados del I.P.N., Unidad IrapuatoCentro de Investigación y de Estudios Avanzados del I.P.N., Unidad IrapuatoUniversidad Autónoma de Nuevo LeónUniversity of CambridgeCentro de Investigación y de Estudios Avanzados del I. P. N., Unidad IrapuatoCentro de Investigación y de Estudios Avanzados del I.P.N., Unidad IrapuatoGrain amaranths tolerate stress and produce highly nutritious seeds. We have identified several (a)biotic stress-responsive genes of unknown function in Amaranthus hypochondriacus, including the so-called Ah24 gene. Ah24 was expressed in young or developing tissues; it was also strongly induced by mechanical damage, insect herbivory and methyl jasmonate and in meristems and newly emerging leaves of severely defoliated plants. Interestingly, an in silico analysis of its 1304 bp promoter region showed a predominance of regulatory boxes involved in development, but not in defense. The Ah24 cDNA encodes a predicted cytosolic protein of 164 amino acids, the localization of which was confirmed by confocal microscopy. Additional in silico analysis identified several other Ah24 homologs, present almost exclusively in plants belonging to the Caryophyllales. The possible function of this gene in planta was examined in transgenic Ah24 overexpressing Arabidopsis thaliana and Nicotiana tabacum plants. Transformed Arabidopsis showed enhanced vegetative growth and increased leaf number with no penalty in one fitness component, such as seed yield, in experimental conditions. Transgenic tobacco plants, which grew and reproduced normally, had increased insect herbivory resistance. Modified vegetative growth in transgenic Arabidopsis coincided with significant changes in the expression of genes controlling phytohormone synthesis or signaling, whereas increased resistance to insect herbivory in transgenic tobacco coincided with higher jasmonic acid and proteinase inhibitor activity levels, plus the accumulation of nicotine and several other putative defense-related metabolites. It is proposed that the primary role of the Ah24 gene in A. hypochondriacus is to contribute to a rapid recovery post-wounding or defoliation, although its participation in defense against insect herbivory is also plausible.http://journal.frontiersin.org/Journal/10.3389/fpls.2015.00602/fulldevelopmentJasmonic aciddefoliationGrain amaranth(A)biotic stresstaxonomically restricted genes
spellingShingle Julio Armando Massange-Sanchez
Paola Andrea Palmeros-Suarez
Norma Angelica Martinez-Gallardo
Paula Andrea Castrillon-Arbelaez
Hamlet eAviles-Arnaut
Fulgencio eAlatorre-Cobo
Axel eTiessen
John Paul Délano-Frier
The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
Frontiers in Plant Science
development
Jasmonic acid
defoliation
Grain amaranth
(A)biotic stress
taxonomically restricted genes
title The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
title_full The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
title_fullStr The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
title_full_unstemmed The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
title_short The novel and taxonomically restricted Ah24 gene from grain amaranth (Amaranthus hypochondriacus) has a dual role in development and defense
title_sort novel and taxonomically restricted ah24 gene from grain amaranth amaranthus hypochondriacus has a dual role in development and defense
topic development
Jasmonic acid
defoliation
Grain amaranth
(A)biotic stress
taxonomically restricted genes
url http://journal.frontiersin.org/Journal/10.3389/fpls.2015.00602/full
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