Spatiotemporal auxin distribution in Arabidopsis tissues is regulated by anabolic and catabolic reactions under long-term ammonium stress
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články
PubMed
34922457
PubMed Central
PMC8684078
DOI
10.1186/s12870-021-03385-9
PII: 10.1186/s12870-021-03385-9
Knihovny.cz E-zdroje
- Klíčová slova
- Ammonium nutrition, Arabidopsis thaliana, Auxin conjugation, Auxin degradation, Auxin synthesis, Root development,
- MeSH
- amoniové sloučeniny metabolismus MeSH
- Arabidopsis metabolismus MeSH
- časoprostorová analýza MeSH
- fyziologický stres MeSH
- kořeny rostlin metabolismus MeSH
- kyseliny indoloctové metabolismus MeSH
- metabolismus MeSH
- oxidace-redukce MeSH
- tkáňová distribuce MeSH
- výhonky rostlin metabolismus MeSH
- Publikační typ
- časopisecké články MeSH
- Názvy látek
- amoniové sloučeniny MeSH
- indoleacetic acid MeSH Prohlížeč
- kyseliny indoloctové MeSH
BACKGROUND: The plant hormone auxin is a major coordinator of plant growth and development in response to diverse environmental signals, including nutritional conditions. Sole ammonium (NH4+) nutrition is one of the unique growth-suppressing conditions for plants. Therefore, the quest to understand NH4+-mediated developmental defects led us to analyze auxin metabolism. RESULTS: Indole-3-acetic acid (IAA), the most predominant natural auxin, accumulates in the leaves and roots of mature Arabidopsis thaliana plants grown on NH4+, but not in the root tips. We found changes at the expressional level in reactions leading to IAA biosynthesis and deactivation in different tissues. Finally, NH4+ nutrition would facilitate the formation of inactive oxidized IAA as the final product. CONCLUSIONS: NH4+-mediated accelerated auxin turnover rates implicate transient and local IAA peaks. A noticeable auxin pattern in tissues correlates with the developmental adaptations of the short and highly branched root system of NH4+-grown plants. Therefore, the spatiotemporal distribution of auxin might be a root-shaping signal specific to adjust to NH4+-stress conditions.
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Luo L, Zhang Y, Xu G. How does nitrogen shape plant architecture? J Exp Bot. 2020;71:4415–4427. PubMed PMC
Bittsánszky A, Pilinszky K, Gyulai G, Komives T. Overcoming ammonium toxicity. Plant Sci. 2015;231:184–190. PubMed
Liu Y, von Wirén N. Ammonium as a signal for physiological and morphological responses in plants. J Exp Bot. 2017;68:2581–2592. PubMed
Britto DT, Kronzucker HJ. NH4+ toxicity in higher plants: a critical review. J Plant Physiol. 2002;159:567–584.
Gerendás J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B. Physiological and biochemical processes related to ammonium toxicity in higher plants. J Plant Nutr Soil Sci. 1997;160:239–251.
Li B, Li G, Kronzucker HJ, Baluška F, Shi W. Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends Plant Sci. 2014;19:107–114. PubMed
Podgórska A, Szal B. The role of reactive oxygen species under ammonium nutrition. In: Gupta KJ, Igamberdiev AU, editors. Reactive oxygen and nitrogen species signaling and communication in plants. Cham: Switzerland Springer International Publishing; 2015. p. 133–53.
Vanneste S, Friml J. Auxin: a trigger for change in plant development. Cell. 2009;20:1005–1016. PubMed
Velasquez SM, Barbez E, Kleine-Vehn J, Estevez JM. Auxin and cellular elongation. Plant Physiol. 2016;170:1206–1215. PubMed PMC
Weijers D, Nemhauser J, Yang Z. Auxin: small molecule, big impact. J Exp Bot. 2018;69:133–136. PubMed PMC
Lavenus J, Goh T, Roberts I, Guyomarc’h S, Lucas M, De Smet I, Fukaki H, Beeckman T, Bennett M, Laplaze L. Lateral root development in Arabidopsis: fifty shades of auxin. Trends Plant Sci. 2013;18:450–458. PubMed
Petrášek J, Elčkner M, Morris DA, Zažimalová E. Auxin efflux carrier activity and auxin accumulation regulate cell division and polarity in tabacco cells. Planta. 2002;216:302–308. PubMed
Vanneste S, Maes L, De Smet I, Himanen K, Naudts M, Inzé D, Beeckman T. Auxin regulation of cell cycle and its role during lateral root initiation. Physiol Plant. 2005;123:139–146.
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. PubMed
Zhao Y. Auxin biosynthesis: a simple two- step pathway converts tryptophan to Indole-3-acetic acid in plants. Mol Plant. 2012;5:334–338. PubMed PMC
Olatunji D, Geelen D, Verstraeten I. Control of endogenous auxin levels in plant root development. Int J Mol Sci. 2017;18:2587. PubMed PMC
Ludwig-Müller J. Auxin conjugates: their role for plant development and in the evolution of land plants. J Exp Bot. 2011;62:1757–1773. PubMed
Mellor N, Band LR, Pěnčík A, Novák O, Rashed A, Holman T, Wilson MH, Voß U, Bishopp A, King JR, Ljung K, Bennett MJ, Owen MR. Dynamic regulation of auxin oxidase and conjugating enzymes AtDAO1 and GH3 modulates auxin homeostasis. Proc Natl Acad Sci U S A. 2016;113:11022–11027. PubMed PMC
Zhang J, Peer WA. Auxin homeostasis: the DAO of catabolism. J Exp Bot. 2017;68:3145–3154. PubMed
Pěnčík A, Simonovik B, Petersson SV, Henyková E, Simon S, Greenham K, Zhang Y, Kowalczyk M, Estelle M, Zazímalová E, Novák O, Sandberg G, Ljung K. Regulation of auxin homeostasis and gradients in Arabidopsis roots through the formation of the indole-3-acetic acid catabolite 2-oxindole-3-acetic acid. Plant Cell. 2013;25:3858–3870. PubMed PMC
Leyser O. Auxin signaling. Plant Physiol. 2017;176:465–479. PubMed PMC
Di DW, Li G, Sun L, Wu J, Wang M, Kronzucker HJ, Fang S, Chu J, Shi W. High ammonium inhibits root growth in Arabidopsis thaliana by promoting auxin conjugation rather than inhibiting auxin biosynthesis. J Plant Physiol. 2021;261:153415. PubMed
Meier M, Liu Y, Lay-Pruitt KS, Takahashi H, von Wirén N. Auxin-mediated root branching is determined by the form of available nitrogen. Nat Plants. 2020;6:1136–1145. PubMed
Li Q, Li BH, Kronzucker HJ, Shi WM. Root growth inhibition by NH4+ in Arabidopsis is mediated by the root tip and is linked to NH4+ efflux and GMPase activity. Plant Cell Environ. 2010;33:1529–1542. PubMed
Liu Y, Lai N, Gao K, Chen F, Yuan L, Mi G. Ammonium inhibits primary root growth by reducing the length of meristem and elongation zone and decreasing elemental expansion rate in the root apex in Arabidopsis thaliana. PLoS One. 2013;8:1–11. PubMed PMC
Yang H, Von der Fecht-Bartenbach J, Friml J, Lohmann J, Neuhäuser B, Ludewig U. Auxin-modulated root growth inhibition in Arabidopsis thaliana seedlings with ammonium as the sole nitrogen source. Funct Plant Biol. 2015;42:239–251. PubMed
Ottenschläger I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K. Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proc Natl Acad Sci U S A. 2003;100:2987–2991. PubMed PMC
Blakeslee JJ, Spatola Rossi T, Kriechbaumer V. Auxin biosynthesis: spatial regulation and adaptation to stress. J Exp Bot. 2019;70:5041–5049. PubMed
Korver RA, Koevoets IT, Testerink C. Out of shape during stress: a key role for auxin. Trends Plant Sci. 2018;23:783–793. PubMed PMC
Podgórska A, Burian M, Gieczewska K, Ostaszewska-Bugajska M, Zebrowski J, Solecka D, Szal B. Altered cell wall plasticity can restrict plant growth under ammonium nutrition. Front Plant Sci. 2017;8:1344. PubMed PMC
Bilsborough GD, Runions A, Barkoulas M, Jenkins HW, Hasson A, Galinha C, Laufs P, Hay A, Prusinkiewicz P, Tsiantis M. Model for the regulation of Arabidopsis thaliana leaf margin development. Proc Natl Acad Sci U S A. 2011;108:3424–3429. PubMed PMC
Brumos J, Robles LM, Yun J, Vu TC, Jackson S, Alonso JM, Stepanova AN. Local auxin biosynthesis is a key regulator of plant development. Dev Cell. 2018;47:306–318.e5. PubMed
Casanova-Sáez R, Voß U. Auxin metabolism controls developmental decisions in land plants. Trends Plant Sci. 2019;24:741–54. PubMed
Lv B, Yan Z, Tian H, Zhang X, Ding Z. Local auxin biosynthesis mediates plant growth and development. Trends Plant Sci. 2019;24:6–9. PubMed
Wang P, Wang Z, Pan Q, Sun X, Chen H, Chen F, Yuan L, Mi G. Increased biomass accumulation in maize grown in mixed nitrogen supply is mediated by auxin synthesis. J Exp Bot. 2019;70:1859-73. 10.1093/jxb/erz047. PubMed PMC
Gao K, Zhou T, Hua Y, Guan C, Zhang Z. Transcription factor WRKY23 is involved in ammonium-induced repression of Arabidopsis primary root growth under ammonium toxicity. Plant Physiol Biochem. 2020;150:90–8. PubMed
Suzuki M, Yamazaki C, Mitsui M, Kakei Y, Mitani Y, Nakamura A, Ishii T, Soeno K, Shimada Y. Transcriptional feedback regulation of YUCCA genes in response to auxin levels in Arabidopsis. Plant Cell Rep. 2015;34:1343–1352. PubMed
Porco S, Pěnčík A, Rashed A, Voß U, Casanova-Sáez R, Bishopp A, Golebiowska A, Bhosale R, Swarup R, Swarup K, Peňáková P, Novák O, Staswick P, Hedden P, Phillips AL, Vissenberg K, Bennett MJ, Ljung K. Dioxygenase-encoding AtDAO1 gene controls IAA oxidation and homeostasis in Arabidopsis. Proc Natl Acad Sci U S A. 2016;113:11016–11021. PubMed PMC
Tanaka K, Hayashi K, Natsume M, Kamiya Y, Sakakibara H, Kawaide H, Kasahara H. UGT74D1 catalyzes the glucosylation of 2-oxindole-3-acetic acid in the auxin metabolic pathway in Arabidopsis. Plant Cell Physiol. 2014;55:218–228. PubMed PMC
Östin A, Kowalyczk M, Bhalerao RP, Sandberg G. Metabolism of indole-3-acetic acid in Arabidopsis. Plant Physiol. 1998;118:285–296. PubMed PMC
Korasick DA, Enders TA, Strader LC. Auxin biosynthesis and storage forms. J Exp Bot. 2013;64:2541–2555. PubMed PMC
Di DW, Sun L, Wang M, Wu J, Kronzucker HJ, Fang S, Chu J, Shi W, Li G. WRKY46 promotes ammonium tolerance in Arabidopsis by repressing NUDX9 and indole-3-acetic acid-conjugating genes and by inhibiting ammonium efflux in the root elongation zone. New Phytol. 2021;32:190–207. PubMed
Di DW, Sun L, Zhang X, et al. Involvement of auxin in the regulation of ammonium tolerance in rice (Oryza sativa L.) Plant Soil. 2018;432:373–387.
Ljung K, Hull AK, Celenza J, Yamada M, Estelle M, Normanly J, Sandberg G. Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell. 2005;17:1090–1104. PubMed PMC
Tian H, De Smet I, Ding Z. Shaping a root system: regulating lateral versus primary root growth. Trends Plant Sci. 2014;19:426–431. PubMed
Chen Q, Dai X, De-Paoli H, Cheng Y, Takebayashi Y, Kasahara H, Kamiya Y, Zhao Y. Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 2014;55:1072–1079. PubMed PMC
Zhang J, Lin JE, Harris C, Campos Mastrotti Pereira F, Wu F, Blakeslee JJ, Peer WA. DAO1 catalyzes temporal and tissue-specific oxidative inactivation of auxin in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2016;113:11010–11015. PubMed PMC
Lima JE, Kojima S, Takahashi H, von Wirén N. Ammonium triggers lateral root branching in Arabidopsis in an AMMONIUM TRANSPORTER1;3-dependent manner. Plant Cell. 2010;22:3621–3633. PubMed PMC
Waidmann S, Sarkel E, Kleine-Vehn J. Same same, but different: growth responses of primary and lateral roots. J Exp Bot. 2020;71:2397–2411. PubMed PMC
Nibau C, Gibbs DJ, Coates JC. Branching out in new directions: the control of root architecture by lateral root formation. New Phytol. 2008;179:595–614. PubMed
Atkinson JA, Rasmussen A, Traini R, Voß U, Sturrock C, Mooney SJ, Wells DM, Bennett MJ. Branching out in roots: uncovering form, function, and regulation. Plant Physiol. 2014;166:538–550. PubMed PMC
Zilio M, Motta S, Tambone F, Scaglia B, Boccasile G, Squartini A, Adani F. The distribution of functional N-cycle related genes and ammonia and nitrate nitrogen in soil profiles fertilized with mineral and organic N fertilizer. PLoS One. 2020;15:e0228364. PubMed PMC
Jia Z, von Wirén N. Signaling pathways underlying nitrogen-dependent changes in root system architecture: from model to crop species. J Exp Bot. 2020;71:4393–4404. PubMed PMC
Nacry P, Bouguyon E, Gojon A. Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil. 2013;370:1–29.
Murashige T, Skoog F. A revised medium for rapid growth and bioassay with tobacco tissue cultures. Physiol Plant. 1962;15:473–497.
Podgórska A, Gieczewska K, Łukawska-Kuźma K, Rasmusson AG, Gardeström P, Szal B. Long-term ammonium nutrition of Arabidopsis increases the extrachloroplastic NAD(P)H/NAD(P)+ ratio and mitochondrial reactive oxygen species level in leaves but does not impair photosynthetic capacity. Plant Cell Environ. 2013;36:2034–2045. PubMed
Barabasz A, Palusińska M, Papierniak A, Kendziorek M, Kozak K, Williams LE, Antosiewicz DM. Functional analysis of NtZIP4B and Zn status-dependent expression pattern of tobacco ZIP genes. Front Plant Sci. 2019;9:1984. PubMed PMC
Escobar MA, Franklin KA, Svensson AS, Salter MG, Whitelam GC, Rasmusson AG. Light regulation of the Arabidopsis respiratory chain. Multiple discrete photoreceptor responses contribute to induction of type II NAD(P)H dehydrogenase genes. Plant Physiol. 2004;136:2710–2721. PubMed PMC
Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol. 2005;139:5–17. PubMed PMC
Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant J. 2012;72:523–536. PubMed