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

Massange-Sanchez JA, Palmeros-Suarez PA, Martinez-Gallardo NA, Castrillon-Arbelaez PA, Avilés-Arnaut H, Alatorre-Cobos F, Tiessen A, Délano-Frier JP - Front Plant Sci (2015)

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Biotechnology and Biochemistry Department, Centro de Investigación y de Estudios Avanzados del I. P. N., Unidad Irapuato Irapuato, México.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

The overexpression (OE) of Ah24 in transgenic Arabidopsis plants enhances vegetative growth and increases leaf number. (A) The rosette size of the three lines of transgenic Arabidopsis plants tested (L15, L11, and L5) is visibly larger than WT controls. Bars and error bars represent the mean values ± SE of (B) the fresh (FW) and dry weights (DW) of the rosette (Rt), inflorescence (In) and aerial tissue (At: Rt + In) of mature Ah24 OE transgenic (L15, gray; L11, black, and L5, striped) and WT (empty bars) Arabidopsis plants, and of (C) the leaf number in mature transgenic Ah24 OE (L15, L11, and L5) and untransformed (WT) plants. All data was obtained using 10 plants per analysis (n = 10). Different letters over the bars represent statistically significant differences at P ≤ 0.05 (Tukey–Kramer test).
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Figure 8: The overexpression (OE) of Ah24 in transgenic Arabidopsis plants enhances vegetative growth and increases leaf number. (A) The rosette size of the three lines of transgenic Arabidopsis plants tested (L15, L11, and L5) is visibly larger than WT controls. Bars and error bars represent the mean values ± SE of (B) the fresh (FW) and dry weights (DW) of the rosette (Rt), inflorescence (In) and aerial tissue (At: Rt + In) of mature Ah24 OE transgenic (L15, gray; L11, black, and L5, striped) and WT (empty bars) Arabidopsis plants, and of (C) the leaf number in mature transgenic Ah24 OE (L15, L11, and L5) and untransformed (WT) plants. All data was obtained using 10 plants per analysis (n = 10). Different letters over the bars represent statistically significant differences at P ≤ 0.05 (Tukey–Kramer test).

Mentions: Seven Arabidopsis T2 homozygous OE transgenic lines with a single T-DNA insertion were randomly selected. They showed significantly different Ah24 expression levels, ranging from 1 × 104 to 5 × 105-fold higher expression levels relative to background expression levels in untransformed controls (Figure S5 in Supplementary Materials). Three lines with differing Ah24 expression levels [high (L15), middle (L11), and low (L5)] were selected for further experimentation. In most experiments, Ah24 expression dosage in transgenic OE Arabidopsis lines significantly affected their vegetative and reproductive growth. The primary roots of the three OE lines were significantly shorter than the WT controls as measured in 2- to 9-day-old seedlings (Figures 6A,B). However, this tendency was reversed as plants developed, since roots tended to be larger and had a higher fresh and dry weights in 6-week-old OE transgenic plants (Figures 6C–E). WT and OE plants bolted after 3 weeks of growth and developed a main stem. No difference in flowering time (i.e., 3.5 weeks ± 1 day) was detected between WT and OE plants. However, the length of the main stem was inversely correlated with the level of Ah24 transgene expression, as shown in Figure 7A. Also, this negative effect was corrected as plants became older, since stem size in the L15 line became indistinguishable from WT plants (Figure 7B). Conversely, rosette sizes in OE plants were visibly larger, as confirmed by their significantly higher rosette and inflorescence fresh and dry masses (Figures 8A,B). Surprisingly, leaf number was significantly higher in all three transgenic OE lines tested (Figure 8C). These changes in vegetative development did not impose a fitness cost in terms of reproductive development since no differences in seed yield were observed between WT and transgenic OE plants (Figure S6 in Supplementary Materials).


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

Massange-Sanchez JA, Palmeros-Suarez PA, Martinez-Gallardo NA, Castrillon-Arbelaez PA, Avilés-Arnaut H, Alatorre-Cobos F, Tiessen A, Délano-Frier JP - Front Plant Sci (2015)

The overexpression (OE) of Ah24 in transgenic Arabidopsis plants enhances vegetative growth and increases leaf number. (A) The rosette size of the three lines of transgenic Arabidopsis plants tested (L15, L11, and L5) is visibly larger than WT controls. Bars and error bars represent the mean values ± SE of (B) the fresh (FW) and dry weights (DW) of the rosette (Rt), inflorescence (In) and aerial tissue (At: Rt + In) of mature Ah24 OE transgenic (L15, gray; L11, black, and L5, striped) and WT (empty bars) Arabidopsis plants, and of (C) the leaf number in mature transgenic Ah24 OE (L15, L11, and L5) and untransformed (WT) plants. All data was obtained using 10 plants per analysis (n = 10). Different letters over the bars represent statistically significant differences at P ≤ 0.05 (Tukey–Kramer test).
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Figure 8: The overexpression (OE) of Ah24 in transgenic Arabidopsis plants enhances vegetative growth and increases leaf number. (A) The rosette size of the three lines of transgenic Arabidopsis plants tested (L15, L11, and L5) is visibly larger than WT controls. Bars and error bars represent the mean values ± SE of (B) the fresh (FW) and dry weights (DW) of the rosette (Rt), inflorescence (In) and aerial tissue (At: Rt + In) of mature Ah24 OE transgenic (L15, gray; L11, black, and L5, striped) and WT (empty bars) Arabidopsis plants, and of (C) the leaf number in mature transgenic Ah24 OE (L15, L11, and L5) and untransformed (WT) plants. All data was obtained using 10 plants per analysis (n = 10). Different letters over the bars represent statistically significant differences at P ≤ 0.05 (Tukey–Kramer test).
Mentions: Seven Arabidopsis T2 homozygous OE transgenic lines with a single T-DNA insertion were randomly selected. They showed significantly different Ah24 expression levels, ranging from 1 × 104 to 5 × 105-fold higher expression levels relative to background expression levels in untransformed controls (Figure S5 in Supplementary Materials). Three lines with differing Ah24 expression levels [high (L15), middle (L11), and low (L5)] were selected for further experimentation. In most experiments, Ah24 expression dosage in transgenic OE Arabidopsis lines significantly affected their vegetative and reproductive growth. The primary roots of the three OE lines were significantly shorter than the WT controls as measured in 2- to 9-day-old seedlings (Figures 6A,B). However, this tendency was reversed as plants developed, since roots tended to be larger and had a higher fresh and dry weights in 6-week-old OE transgenic plants (Figures 6C–E). WT and OE plants bolted after 3 weeks of growth and developed a main stem. No difference in flowering time (i.e., 3.5 weeks ± 1 day) was detected between WT and OE plants. However, the length of the main stem was inversely correlated with the level of Ah24 transgene expression, as shown in Figure 7A. Also, this negative effect was corrected as plants became older, since stem size in the L15 line became indistinguishable from WT plants (Figure 7B). Conversely, rosette sizes in OE plants were visibly larger, as confirmed by their significantly higher rosette and inflorescence fresh and dry masses (Figures 8A,B). Surprisingly, leaf number was significantly higher in all three transgenic OE lines tested (Figure 8C). These changes in vegetative development did not impose a fitness cost in terms of reproductive development since no differences in seed yield were observed between WT and transgenic OE plants (Figure S6 in Supplementary Materials).

Bottom Line: 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.

View Article: PubMed Central - PubMed

Affiliation: Biotechnology and Biochemistry Department, Centro de Investigación y de Estudios Avanzados del I. P. N., Unidad Irapuato Irapuato, México.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus