IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress

Natsuko Kinoshita; Huan Wang; Hiroyuki Kasahara; Jun Liu; Cameron R. MacPherson; Yasunori Machida; Yuji Kamiya; Matthew A. Hannah; Nam Hai Chuaa

doi:10.1105/tpc.112.097006

IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress

Natsuko Kinoshita, Huan Wang, Hiroyuki Kasahara, Jun Liu, Cameron R. MacPherson, Yasunori Machida, Yuji Kamiya, Matthew A. Hannah, Nam Hai Chuaa

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199 Scopus citations

Abstract

The functions of microRNAs and their target mRNAs in Arabidopsis thaliana development have been widely documented; however, roles of stress-responsive microRNAs and their targets are not as well understood. Using small RNA deep sequencing and ATH1 microarrays to profile mRNAs, we identified IAA-Ala Resistant3 (IAR3) as a new target of miR167a. As expected, IAR3 mRNA was cleaved at the miR167a complementary site and under high osmotic stress miR167a levels decreased, whereas IAR3 mRNA levels increased. IAR3 hydrolyzes an inactive form of auxin (indole-3-acetic acid [IAA]-alanine) and releases bioactive auxin (IAA), a central phytohormone for root development. In contrast with the wild type, iar3 mutants accumulated reduced IAA levels and did not display high osmotic stress-induced root architecture changes. Transgenic plants expressing a cleavage-resistant form of IAR3 mRNA accumulated high levels of IAR3 mRNAs and showed increased lateral root development compared with transgenic plants expressing wild-type IAR3. Expression of an inducible noncoding RNA to sequester miR167a by target mimicry led to an increase in IAR3 mRNA levels, further confirming the inverse relationship between the two partners. Sequence comparison revealed the miR167 target site on IAR3 mRNA is conserved in evolutionarily distant plant species. Finally, we showed that IAR3 is required for drought tolerance. © 2012 American Society of Plant Biologists. All rights reserved.

Original language	English (US)
Pages (from-to)	3590-3602
Number of pages	13
Journal	The Plant Cell
Volume	24
Issue number	9
DOIs	https://doi.org/10.1105/tpc.112.097006
State	Published - Sep 7 2012

Bibliographical note

KAUST Repository Item: Exported on 2020-10-01
Acknowledgements: We thank Jason Reed for the generous gifts of arf6-2 and arf8-3 single mutant and arf6-2 arf8-3 double mutant seeds, our laboratory members for discussions, Nagarajan Chandramouli of Rockefeller Proteomics Resource Center for sample preparation relating to free IAA measurement, and Scott Dewell of the Genomics Resource Center for deep sequencing. N.K. was supported by postdoctoral fellowships from the Uehara Memorial Foundation, Swiss National Science Foundation (for Prospective Researchers), and the Japan Society for the Promotion of Science. This work was supported in part by Bayer Crop Science and in part by the Cooperative Research Program for Agricultural Science and Technology Development (PJ906910), Rural Development Administration, Republic of Korea.

ASJC Scopus subject areas

Plant Science
Cell Biology

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10.1105/tpc.112.097006

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@article{26e844dcc6a145928df6b1141f92526f,

title = "IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress",

abstract = "The functions of microRNAs and their target mRNAs in Arabidopsis thaliana development have been widely documented; however, roles of stress-responsive microRNAs and their targets are not as well understood. Using small RNA deep sequencing and ATH1 microarrays to profile mRNAs, we identified IAA-Ala Resistant3 (IAR3) as a new target of miR167a. As expected, IAR3 mRNA was cleaved at the miR167a complementary site and under high osmotic stress miR167a levels decreased, whereas IAR3 mRNA levels increased. IAR3 hydrolyzes an inactive form of auxin (indole-3-acetic acid [IAA]-alanine) and releases bioactive auxin (IAA), a central phytohormone for root development. In contrast with the wild type, iar3 mutants accumulated reduced IAA levels and did not display high osmotic stress-induced root architecture changes. Transgenic plants expressing a cleavage-resistant form of IAR3 mRNA accumulated high levels of IAR3 mRNAs and showed increased lateral root development compared with transgenic plants expressing wild-type IAR3. Expression of an inducible noncoding RNA to sequester miR167a by target mimicry led to an increase in IAR3 mRNA levels, further confirming the inverse relationship between the two partners. Sequence comparison revealed the miR167 target site on IAR3 mRNA is conserved in evolutionarily distant plant species. Finally, we showed that IAR3 is required for drought tolerance. {\textcopyright} 2012 American Society of Plant Biologists. All rights reserved.",

author = "Natsuko Kinoshita and Huan Wang and Hiroyuki Kasahara and Jun Liu and MacPherson, {Cameron R.} and Yasunori Machida and Yuji Kamiya and Hannah, {Matthew A.} and Chuaa, {Nam Hai}",

note = "KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Jason Reed for the generous gifts of arf6-2 and arf8-3 single mutant and arf6-2 arf8-3 double mutant seeds, our laboratory members for discussions, Nagarajan Chandramouli of Rockefeller Proteomics Resource Center for sample preparation relating to free IAA measurement, and Scott Dewell of the Genomics Resource Center for deep sequencing. N.K. was supported by postdoctoral fellowships from the Uehara Memorial Foundation, Swiss National Science Foundation (for Prospective Researchers), and the Japan Society for the Promotion of Science. This work was supported in part by Bayer Crop Science and in part by the Cooperative Research Program for Agricultural Science and Technology Development (PJ906910), Rural Development Administration, Republic of Korea.",

year = "2012",

month = sep,

day = "7",

doi = "10.1105/tpc.112.097006",

language = "English (US)",

volume = "24",

pages = "3590--3602",

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T1 - IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress

AU - Kinoshita, Natsuko

AU - Wang, Huan

AU - Kasahara, Hiroyuki

AU - Liu, Jun

AU - MacPherson, Cameron R.

AU - Machida, Yasunori

AU - Kamiya, Yuji

AU - Hannah, Matthew A.

AU - Chuaa, Nam Hai

N1 - KAUST Repository Item: Exported on 2020-10-01 Acknowledgements: We thank Jason Reed for the generous gifts of arf6-2 and arf8-3 single mutant and arf6-2 arf8-3 double mutant seeds, our laboratory members for discussions, Nagarajan Chandramouli of Rockefeller Proteomics Resource Center for sample preparation relating to free IAA measurement, and Scott Dewell of the Genomics Resource Center for deep sequencing. N.K. was supported by postdoctoral fellowships from the Uehara Memorial Foundation, Swiss National Science Foundation (for Prospective Researchers), and the Japan Society for the Promotion of Science. This work was supported in part by Bayer Crop Science and in part by the Cooperative Research Program for Agricultural Science and Technology Development (PJ906910), Rural Development Administration, Republic of Korea.

PY - 2012/9/7

Y1 - 2012/9/7

N2 - The functions of microRNAs and their target mRNAs in Arabidopsis thaliana development have been widely documented; however, roles of stress-responsive microRNAs and their targets are not as well understood. Using small RNA deep sequencing and ATH1 microarrays to profile mRNAs, we identified IAA-Ala Resistant3 (IAR3) as a new target of miR167a. As expected, IAR3 mRNA was cleaved at the miR167a complementary site and under high osmotic stress miR167a levels decreased, whereas IAR3 mRNA levels increased. IAR3 hydrolyzes an inactive form of auxin (indole-3-acetic acid [IAA]-alanine) and releases bioactive auxin (IAA), a central phytohormone for root development. In contrast with the wild type, iar3 mutants accumulated reduced IAA levels and did not display high osmotic stress-induced root architecture changes. Transgenic plants expressing a cleavage-resistant form of IAR3 mRNA accumulated high levels of IAR3 mRNAs and showed increased lateral root development compared with transgenic plants expressing wild-type IAR3. Expression of an inducible noncoding RNA to sequester miR167a by target mimicry led to an increase in IAR3 mRNA levels, further confirming the inverse relationship between the two partners. Sequence comparison revealed the miR167 target site on IAR3 mRNA is conserved in evolutionarily distant plant species. Finally, we showed that IAR3 is required for drought tolerance. © 2012 American Society of Plant Biologists. All rights reserved.

AB - The functions of microRNAs and their target mRNAs in Arabidopsis thaliana development have been widely documented; however, roles of stress-responsive microRNAs and their targets are not as well understood. Using small RNA deep sequencing and ATH1 microarrays to profile mRNAs, we identified IAA-Ala Resistant3 (IAR3) as a new target of miR167a. As expected, IAR3 mRNA was cleaved at the miR167a complementary site and under high osmotic stress miR167a levels decreased, whereas IAR3 mRNA levels increased. IAR3 hydrolyzes an inactive form of auxin (indole-3-acetic acid [IAA]-alanine) and releases bioactive auxin (IAA), a central phytohormone for root development. In contrast with the wild type, iar3 mutants accumulated reduced IAA levels and did not display high osmotic stress-induced root architecture changes. Transgenic plants expressing a cleavage-resistant form of IAR3 mRNA accumulated high levels of IAR3 mRNAs and showed increased lateral root development compared with transgenic plants expressing wild-type IAR3. Expression of an inducible noncoding RNA to sequester miR167a by target mimicry led to an increase in IAR3 mRNA levels, further confirming the inverse relationship between the two partners. Sequence comparison revealed the miR167 target site on IAR3 mRNA is conserved in evolutionarily distant plant species. Finally, we showed that IAR3 is required for drought tolerance. © 2012 American Society of Plant Biologists. All rights reserved.

UR - http://hdl.handle.net/10754/562315

UR - http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3480289

UR - http://www.scopus.com/inward/record.url?scp=84868116999&partnerID=8YFLogxK

U2 - 10.1105/tpc.112.097006

DO - 10.1105/tpc.112.097006

M3 - Article

C2 - 22960911

SN - 1040-4651

VL - 24

SP - 3590

EP - 3602

JO - The Plant Cell

JF - The Plant Cell

IS - 9

ER -

IAA-Ala Resistant3, an evolutionarily conserved target of miR167, mediates Arabidopsis root architecture changes during high osmotic stress

Abstract

Bibliographical note

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