Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat

Alberto Casartelli; Vanessa J. Melino; Ute Baumann; Matteo Riboni; Radoslaw Suchecki; Nirupama S. Jayasinghe; Himasha Mendis; Mutsumi Watanabe; Alexander Erban; Ellen Zuther; Rainer Hoefgen; Ute Roessner; Mamoru Okamoto; Sigrid Heuer

doi:10.1007/s11103-019-00831-z

Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat

Alberto Casartelli, Vanessa J. Melino, Ute Baumann, Matteo Riboni, Radoslaw Suchecki, Nirupama S. Jayasinghe, Himasha Mendis, Mutsumi Watanabe, Alexander Erban, Ellen Zuther, Rainer Hoefgen, Ute Roessner, Mamoru Okamoto, Sigrid Heuer^*

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

38 Citations (Scopus)

Abstract

Key message: Degradation of nitrogen-rich purines is tightly and oppositely regulated under drought and low nitrogen supply in bread wheat. Allantoin is a key target metabolite for improving nitrogen homeostasis under stress. Abstract: The metabolite allantoin is an intermediate of the catabolism of purines (components of nucleotides) and is known for its housekeeping role in nitrogen (N) recycling and also for its function in N transport and storage in nodulated legumes. Allantoin was also shown to differentially accumulate upon abiotic stress in a range of plant species but little is known about its role in cereals. To address this, purine catabolic pathway genes were identified in hexaploid bread wheat and their chromosomal location was experimentally validated. A comparative study of two Australian bread wheat genotypes revealed a highly significant increase of allantoin (up to 29-fold) under drought. In contrast, allantoin significantly decreased (up to 22-fold) in response to N deficiency. The observed changes were accompanied by transcriptional adjustment of key purine catabolic genes, suggesting that the recycling of purine-derived N is tightly regulated under stress. We propose opposite fates of allantoin in plants under stress: the accumulation of allantoin under drought circumvents its degradation to ammonium (NH ₄ ⁺ ) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH ₄ ⁺ liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.

Original language	English
Pages (from-to)	477-497
Number of pages	21
Journal	Plant Molecular Biology
Volume	99
Issue number	4-5
DOIs	https://doi.org/10.1007/s11103-019-00831-z
Publication status	Published - 1 Mar 2019
Externally published	Yes

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Casartelli, A., Melino, V. J., Baumann, U., Riboni, M., Suchecki, R., Jayasinghe, N. S., Mendis, H., Watanabe, M., Erban, A., Zuther, E., Hoefgen, R., Roessner, U., Okamoto, M., & Heuer, S. (2019). Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat. Plant Molecular Biology, 99(4-5), 477-497. https://doi.org/10.1007/s11103-019-00831-z

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title = "Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat",

abstract = " Key message: Degradation of nitrogen-rich purines is tightly and oppositely regulated under drought and low nitrogen supply in bread wheat. Allantoin is a key target metabolite for improving nitrogen homeostasis under stress. Abstract: The metabolite allantoin is an intermediate of the catabolism of purines (components of nucleotides) and is known for its housekeeping role in nitrogen (N) recycling and also for its function in N transport and storage in nodulated legumes. Allantoin was also shown to differentially accumulate upon abiotic stress in a range of plant species but little is known about its role in cereals. To address this, purine catabolic pathway genes were identified in hexaploid bread wheat and their chromosomal location was experimentally validated. A comparative study of two Australian bread wheat genotypes revealed a highly significant increase of allantoin (up to 29-fold) under drought. In contrast, allantoin significantly decreased (up to 22-fold) in response to N deficiency. The observed changes were accompanied by transcriptional adjustment of key purine catabolic genes, suggesting that the recycling of purine-derived N is tightly regulated under stress. We propose opposite fates of allantoin in plants under stress: the accumulation of allantoin under drought circumvents its degradation to ammonium (NH 4 + ) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH 4 + liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.",

keywords = "Allantoin, Drought, Nitrogen deficiency, Nutrient recycling, Purine catabolism, Triticum aestivum",

author = "Alberto Casartelli and Melino, {Vanessa J.} and Ute Baumann and Matteo Riboni and Radoslaw Suchecki and Jayasinghe, {Nirupama S.} and Himasha Mendis and Mutsumi Watanabe and Alexander Erban and Ellen Zuther and Rainer Hoefgen and Ute Roessner and Mamoru Okamoto and Sigrid Heuer",

note = "Publisher Copyright: {\textcopyright} 2019, The Author(s).",

year = "2019",

month = mar,

day = "1",

doi = "10.1007/s11103-019-00831-z",

language = "English",

volume = "99",

pages = "477--497",

journal = "Plant Molecular Biology",

issn = "0167-4412",

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Casartelli, A, Melino, VJ, Baumann, U, Riboni, M, Suchecki, R, Jayasinghe, NS, Mendis, H, Watanabe, M, Erban, A, Zuther, E, Hoefgen, R, Roessner, U, Okamoto, M & Heuer, S 2019, 'Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat', Plant Molecular Biology, vol. 99, no. 4-5, pp. 477-497. https://doi.org/10.1007/s11103-019-00831-z

TY - JOUR

T1 - Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat

AU - Casartelli, Alberto

AU - Melino, Vanessa J.

AU - Baumann, Ute

AU - Riboni, Matteo

AU - Suchecki, Radoslaw

AU - Jayasinghe, Nirupama S.

AU - Mendis, Himasha

AU - Watanabe, Mutsumi

AU - Erban, Alexander

AU - Zuther, Ellen

AU - Hoefgen, Rainer

AU - Roessner, Ute

AU - Okamoto, Mamoru

AU - Heuer, Sigrid

PY - 2019/3/1

Y1 - 2019/3/1

N2 - Key message: Degradation of nitrogen-rich purines is tightly and oppositely regulated under drought and low nitrogen supply in bread wheat. Allantoin is a key target metabolite for improving nitrogen homeostasis under stress. Abstract: The metabolite allantoin is an intermediate of the catabolism of purines (components of nucleotides) and is known for its housekeeping role in nitrogen (N) recycling and also for its function in N transport and storage in nodulated legumes. Allantoin was also shown to differentially accumulate upon abiotic stress in a range of plant species but little is known about its role in cereals. To address this, purine catabolic pathway genes were identified in hexaploid bread wheat and their chromosomal location was experimentally validated. A comparative study of two Australian bread wheat genotypes revealed a highly significant increase of allantoin (up to 29-fold) under drought. In contrast, allantoin significantly decreased (up to 22-fold) in response to N deficiency. The observed changes were accompanied by transcriptional adjustment of key purine catabolic genes, suggesting that the recycling of purine-derived N is tightly regulated under stress. We propose opposite fates of allantoin in plants under stress: the accumulation of allantoin under drought circumvents its degradation to ammonium (NH 4 + ) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH 4 + liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.

AB - Key message: Degradation of nitrogen-rich purines is tightly and oppositely regulated under drought and low nitrogen supply in bread wheat. Allantoin is a key target metabolite for improving nitrogen homeostasis under stress. Abstract: The metabolite allantoin is an intermediate of the catabolism of purines (components of nucleotides) and is known for its housekeeping role in nitrogen (N) recycling and also for its function in N transport and storage in nodulated legumes. Allantoin was also shown to differentially accumulate upon abiotic stress in a range of plant species but little is known about its role in cereals. To address this, purine catabolic pathway genes were identified in hexaploid bread wheat and their chromosomal location was experimentally validated. A comparative study of two Australian bread wheat genotypes revealed a highly significant increase of allantoin (up to 29-fold) under drought. In contrast, allantoin significantly decreased (up to 22-fold) in response to N deficiency. The observed changes were accompanied by transcriptional adjustment of key purine catabolic genes, suggesting that the recycling of purine-derived N is tightly regulated under stress. We propose opposite fates of allantoin in plants under stress: the accumulation of allantoin under drought circumvents its degradation to ammonium (NH 4 + ) thereby preventing N losses. On the other hand, under N deficiency, increasing the NH 4 + liberated via allantoin catabolism contributes towards the maintenance of N homeostasis.

KW - Allantoin

KW - Drought

KW - Nitrogen deficiency

KW - Nutrient recycling

KW - Purine catabolism

KW - Triticum aestivum

UR - http://www.scopus.com/inward/record.url?scp=85061034315&partnerID=8YFLogxK

U2 - 10.1007/s11103-019-00831-z

DO - 10.1007/s11103-019-00831-z

M3 - Article

SN - 0167-4412

VL - 99

SP - 477

EP - 497

JO - Plant Molecular Biology

JF - Plant Molecular Biology

IS - 4-5

ER -

Opposite fates of the purine metabolite allantoin under water and nitrogen limitations in bread wheat

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