Abstract
Key message
Expression pattern indicates that JA biosynthesis pathway via regulating JA levels might control root system architecture to improve nutrient use efficiency (NUE) and N, P, K+ deficiency tolerance in rice.
Abstract
Deficiencies of macronutrients (N, P and K+) and consequent excessive use of fertilizers have dramatically reduced soil fertility. It calls for development of nutrient use efficient plants. Plants combat nutrient deficiencies by altering their root system architecture (RSA) to enhance the acquisition of nutrients from the soil. Amongst various phytohormones, Jasmonic acid (JA) is known to regulate plant root growth and modulate RSA. Therefore, to understand the role of JA in macronutrient deficiency in rice, expression pattern of JA biosynthesis genes was analyzed under N, P and K+ deficiencies. Several members belonging to different families of JA biosynthesis genes (PLA1, LOX, AOS, AOC, OPR, ACX and JAR1) showed differential expression exclusively in one nutrient deficiency or in multiple nutrient deficiencies. Expression analysis during developmental stages showed that several genes expressed significantly in vegetative tissues, particularly in root. In addition, JA biosynthesis genes were found to have significant expression under the treatment of different phytohormones, including Auxin, cytokinin, gibberellic acid (GA), abscisic acid (ABA), JA and abiotic stresses, such as drought, salinity and cold. Analysis of promoters of these genes revealed various cis-regulatory elements associated with hormone response, plant development and abiotic stresses. These findings suggest that JA biosynthesis pathway by regulating the level of JA might control the RSA thus, it may help rice plant in combating macronutrient deficiency.
Similar content being viewed by others
References
Agrawal GK, Tamogami S, Han O, Iwahashi H, Rakwal R (2004) Rice octadecanoid pathway. Biochem Biophys Res Commun 317:1–15
Aleman F, Yazaki J, Lee M, Takahashi Y, Kim AY, Li Z, Kinoshita T, Ecker JR, Schroeder JI (2016) An ABA-increased interaction of the PYL6 ABA receptor with MYC2 transcription factor: a putative link of ABA and JA signaling. Sci Rep 6:28941
Armengaud P, Breitling R, Amtmann A (2004) The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol 136:2556–2576
Asif I, Qiang D, Xiangru W, Huiping G, Hengheng Z, Xiling Z, Meizhen S (2020) High nitrogen enhance drought tolerance in cotton. Plants 9:2–22
Baker SS, Wilhelm KS, Thomashow MF (1994) The 5’-region of Arabidopsis thaliana cor15a has cis-acting elements that confer cold-, drought- and ABA-regulated gene expression. Plant Mol Biol 24:701–713
Balcerowicz D, Schoenaers S, Vissenberg K (2015) Cell fate determination and the switch from diffuse growth to planar polarity in Arabidopsis root epidermal cells. Front Plant Sci 6:1163
Bannenberg G, Martínez M, Hamberg M, Castresana C (2008) Diversity of the enzymatic activity in the Lipoxygenase gene family of Arabidopsis thaliana. Lipids 44:85
Bhosale R, Giri J, Pandey BK et al (2018) A mechanistic framework for auxin dependent Arabidopsis root hair elongation to low external phosphate. Nat Commun 9:1409
Breeze E, Harrison E, McHattie S et al (2011) High-resolution temporal profiling of transcripts during Arabidopsis leaf senescence reveals a distinct chronology of processes and regulation. Plant Cell 23:873–894
Cai XT, Xu P, Zhao PX, Liu R, Yu LH, Bin Xiang C (2014) Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation. Nat Commun 5:5833
Caldelari D, Wang G, Farmer EE, Dong X (2011) Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol Biol 75:25–33
Chehab EW, Yao C, Henderson Z, Kim S, Braam J (2012) Arabidopsis touch-induced morphogenesis is jasmonate mediated and protects against pests. Curr Biol 22:701–706
Chen Q, Sun J, Zhai Q, Zhou W, Qi L, Xu L, Wang B, Chen R, Jiang H, Qi J, Li X, Palme K, Lia C (2011) The basic helix-loop-helix transcription factor myc2 directly represses plethora expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 23:3335–3352
Chen J, Sonobe K, Ogawa N, Masuda S, Nagatani A, Kobayashi Y, Ohta H (2013a) Inhibition of Arabidopsis hypocotyl elongation by jasmonates is enhanced under red light in phytochrome B dependent manner. J Plant Res 126:161–168
Chen G, Greer MS, Weselake RJ (2013b) Plant phospholipase A: advances in molecular biology, biochemistry, and cellular function. Biomol Concepts 4:527–532
Chen HY, Hsieh EJ, Cheng MC, Chen CY, Hwang SY, Lin TP (2016a) ORA47 (octadecanoid-responsive AP2/ERF-domain transcription factor 47) regulates jasmonic acid and abscisic acid biosynthesis and signaling through binding to a novel cis-element. New Phytol 211:599–613
Chen Y, Ma J, Miller AJ, Luo B, Wang M, Zhu Z, Ouwerkerk PBF (2016b) OsCHX14 is involved in the K+ homeostasis in rice (Oryza sativa) flowers. Plant Cell Physiol 57:1530–1543
Cochrane TT, Cochrane TA (2009) The vital role of potassium in the osmotic mechanism of stomata aperture modulation and its link with potassium deficiency. Plant Signal Behav 4:240–243
Conesa CM, Saez A, Navarro-Neila S, de Lorenzo L, Hunt AG, Sepúlveda EB, Baigorri R, Garcia-Mina JM, Zamarreño AM, Sacristán S, Del Pozo JC (2020) Alternative polyadenylation and salicylic acid modulate root responses to low nitrogen availability. Plants 9(2):251
Coskun D, Britto DT, Kronzucker HJ (2017) The nitrogen–potassium intersection: membranes, metabolism, and mechanism. Plant Cell Environ 40:2029–2041
DeBang TC, Husted S, Laursen KH, Persson DP, Schjoerring JK (2021) The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants. New Phytol 229(5):2446–2469
Dhillon JS, Eickhoff EM, Mullen RW, Raun WR (2019) World potassium use efficiency in cereal crops. Agron J 111:889–896
Diaz-De-Leon F, Klotz KL, Lagrimini LM (1993) Nucleotide sequence of the tobacco (Nicotiana tabacum) anionic peroxidase gene. Plant Physiol 101:1117–1118
Ding L, Gao C, Li Y, Li Y, Zhu Y, Xu G, Shen Q, Kaldenhoff R, Kai L, Guo S (2015) The enhanced drought tolerance of rice plants under ammonium is related to aquaporin (AQP). Plant Sci 234:14–21
Dobermann A, Cassman KG, Mamaril CP, Sheehy JE (1998) Management of phosphorus, potassium, and sulfur in intensive, irrigated lowland rice. Field Crops Res 56:113–138
Du XQ, Wang FL, Li H, Jing S, Yu M, Li J, Wu WH, Kudla J, Wang Y (2019) The transcription factor MYB59 regulates K+/NO3− translocation in the Arabidopsis response to low K+ stress. Plant Cell 31:699–714
Fageria NK (2009) The use of nutrients in crop plants. CRC Press (ISBN 9780367386887)
Farjad M, Rigault M, Pateyron S, Martin-Magniette ML, Krapp A, Meyer C, Fagard M (2018) Nitrogen limitation alters the response of specific genes to biotic stress. Int J Mol Sci 19(11):3364
Faustino LI, Bulfe NML, Pinazo MA, Monteoliva SE, Graciano C (2013) Dry weight partitioning and hydraulic traits in young Pinus taeda trees fertilized with nitrogen and phosphorus in a subtropical area. Tree Physiol 33:241–251
Fernández-Calvo P, Chini A, Fernández-Barbero G et al (2011) The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23:701–715
Feussner I, Wasternack C (2002) The lipoxygenase pathway. Annu Rev Plant Biol 53:275–297
Frank S, Tiemeyer B, Gelbrecht J, Freibauer A, Fisheries I (2014) High soil solution carbon and nitrogen concentrations in a drained Atlantic bog are reduced to natural levels by 10 years of rewetting. Biogeosciences 11:2309–2324
Frink CR, Waggoner PE, Ausubel JH (1999) Perspective nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci USA 96:1175–1180
Gasperini D, Chételat A, Acosta IF, Goossens J, Pauwels L, Goossens A, Dreos R, Alfonso E, Farmer EE (2015) Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet 11(6):e1005300
Giri J, Bhosale R, Huang G et al (2018) Rice auxin influx carrier OsAUX1 facilitates root hair elongation in response to low external phosphate. Nat Commun 9(1):1408
Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C, Hause B (2012) Role of cis-12-Oxo-phytodienoic acid in tomato embryo development. Plant Physiol 158:1715–1727
Gong Z, Xiong L, Shi H et al (2020) Plant abiotic stress response and nutrient use efficiency. Sci China Life Sci 63:635–674
Gruber BD, Giehl RFH, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol 163:161–179
Guida Dos Santos M, Ribeiro RV, Ferraz De Oliveira R, Pimentel C (2004) Gas exchange and yield response to foliar phosphorus application in Phaseolus vulgaris L. under drought. Braz J Plant Physiol 16:171–179
Gutierrez L, Mongelard G, Floková K, Pǎcurar DI, Novák O, Staswick P, Kowalczyk M, Pǎcurar M, Demailly H, Geiss G, Bellini C (2012) Auxin controls Arabidopsis adventitious root initiation by regulating jasmonic acid homeostasis. Plant Cell 24:2515–2527
Haefele SM, NelsonA HRJ (2014) Soil quality and constraints in global rice production. Geoderma 235:250–259
Hafsi C, Debez A, Abdelly C (2014) Potassium deficiency in plants: effects and signaling cascades. Acta Physiol Plant 36:1055–1070
Halford NG (2009) New insights on the effects of heat stress on crops. J Exp Bot 60:4215–4216
Han X, Zhang M, Yang M, Hu Y (2020) Arabidopsis JAZ proteins interact with and suppress RHD6 transcription factor to regulate jasmonate-stimulated root hair development. Plant Cell 32:1049–1062
Hasanuzzaman M, Bhuyan MHMB, Nahar K, Hossain MS, Al Mahmud J, Hossen MS, Masud AAC, Moumita FM (2018) Potassium: a vital regulator of plant responses and tolerance to abiotic stresses. Agronomy 8(3):31
He Y, Gan S (2001) Identical promoter elements are involved in regulation of the OPR1 gene by senescence and jasmonic acid in Arabidopsis. Plant Mol Biol 47:595–605
He Y, Fukushige H, Hildebrand DF, Gan S (2002) Evidence supporting a role of jasmonic acid in Arabidopsis leaf senescence. Plant Physiol 128:876–884
Ho CH, Lin SH, Hu HC, Tsay YF (2009) CHL1 functions as a nitrate sensor in plants. Cell 138:1184–1194
Howe GA, Major IT, Koo AJ (2018) Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol 69:387–415
Hu B, Chu C (2020) Nitrogen–phosphorus interplay: old story with molecular tale. New Phytol 225:1455–1460
Hu B, Jiang Z, Wang W et al (2019) Nitrate–NRT1.1B–SPX4 cascade integrates nitrogen and phosphorus signalling networks in plants. Nat Plants 5:401–413
Huang J, Cai M, Long Q, Liu L, Lin Q, Jiang L, Chen S, Wan J (2014) OsLOX2, a rice type I lipoxygenase, confers opposite effects on seed germination and longevity. Transgenic Res 23:643–655
Huang H, Liu B, Liu L, Song S (2017) Jasmonate action in plant growth and development. J Exp Bot 68:1349–1359
Huang KL, Ma GJ, Zhang ML, Xiong H, Wu H, Zhao CZ, Liu CS, Jia HX, Chen L, Kjorven JO, Li XB, Ren F (2018) The ARF7 and ARF19 transcription factors positively regulate PHOSPHATE STARVATION RESPONSE1 in Arabidopsis roots. Plant Physiol 178:413–427
Ishiguro S, Kawai-Oda A, Ueda J, Nishida I, Okada K (2001) The DEFECTIVE IN ANTHER DEHISCENCE1 gene encodes a novel phospholipase a1 catalyzing the initial step of jasmonic acid biosynthesis, which synchronizes pollen maturation, anther dehiscence, and flower opening in Arabidopsis. Plant Cell 13:2191
Islam A, Muttaleb A (2016) Effect of potassium fertilization on yield and potassium nutrition of Boro rice in a wetland ecosystem of Bangladesh. Arch Agron Soil Sci 62:1530–1540
Islam N, Farhad S, Bhuiyan M, Islam MN, Farhad ISM, Islam MN, Hoque S, Bhuiyan MSI (2010) Role of potassium and sulphur on the growth, yield and oil content of soybean (Glycine max L.). Acad J Plant Sci 3:99–103
Islam A, Chandrabiswas J, Sirajul Karim AJM, Salmapervin M, Saleque AMA (2017) Effects of potassium fertilization on growth and yield of wetland rice in grey terrace soils of Bangladesh. Res Crop Ecophysiol 10:64–82
Itzhaki H, Woodson WR (1993) Characterization of an ethylene-responsive glutathione S-transferase gene cluster in carnation. Plant Mol Biol 22:43–58
Jiang Y, Duan Y, Yin J, Ye S, Zhu J, Zhang F, Lu W, Fan D, Luo K (2014) Genome-wide identification and characterization of the Populus WRKY transcription factor family and analysis of their expression in response to biotic and abiotic stresses. J Exp Bot 65:6629–6644
Jung JY, Shin R, Schachtman DP (2009) Ethylene mediates response and tolerance to potassium deprivation in Arabidopsis. Plant Cell 21:607–621
Kanai S, Moghaieb RE, El-Shemy HA, Panigrahi R, Mohapatra PK, Ito J, Nguyen NT, Saneoka H, Fujita K (2011) Potassium deficiency affects water status and photosynthetic rate of the vegetative sink in green house tomato prior to its effects on source activity. Plant Sci 180:368–374
Khan R, Gurmani AR, Gurmani AH, Zia MS (2007) Effect of potassium application on crop yields under wheat rice system. Sarhad J Agric 23:277–299
Khan GA, Vogiatzaki E, Glauser G, Poirier Y (2016) Phosphate deficiency induces the jasmonate pathway and enhances resistance to insect herbivory. Plant Physiol 171:632–644
Kiba T, Inaba J, Kudo T et al (2018) Repression of nitrogen starvation responses by members of the Arabidopsis GARP-type transcription factor NIGT1/HRS1 subfamily. Plant Cell 30:925–945
Koo AJK, Cooke TF, Howe GA (2011) Cytochrome P450 CYP94B3 mediates catabolism and inactivation of the plant hormone jasmonoyl-l-isoleucine. Proc Natl Acad Sci USA 108:9298–9303
Krouk G, Ruffel S, Gutiérrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16:178–182
Li L, Kim BG, Cheong YH, Pandey GK, Luan S (2006) A Ca2+ signaling pathway regulates a K+ channel for low-K response in Arabidopsis. Proc Natl Acad Sci USA 103:12625–12630
Li JY, Fu YL, Pike SM et al (2010) The Arabidopsis nitrate transporter NRT1.8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. Plant Cell 22:1633–1646
Li G, Wu Y, Liu G, Xiao X, Wang P, Gao T, Xu M, Han Q, Wang Y, Guo T, Kang G (2017a) Large-scale proteomics combined with transgenic experiments demonstrates an important role of jasmonic acid in potassium deficiency response in wheat and rice. Mol Cell Proteomics 16:1889–1905
Li H, Yu M, Du XQ, Wang ZF, Wu WH, Quintero FJ, Jin XH, Li HD, Wang Y (2017b) NRT1.5/NPF7.3 functions as a proton-coupled H+/K+ antiporter for K+ loading into the xylem in Arabidopsis. Plant Cell 29:2016–2026
Li J, Wu WH, Wang Y (2017c) Potassium channel AKT1 is involved in the auxin-mediated root growth inhibition in Arabidopsis response to low K(+) stress. J Integr Plant Biol 59:895–909
Li X, Chen L, Forde BG, Davies WJ (2017d) The biphasic root growth response to abscisic acid in Arabidopsis involves interaction with ethylene and auxin signalling pathways. Front Plant Sci 8:1493
Lin SH, Kuo HF, Canivenc G, Lin CS, Lepetit M, Hsu PK, Tillard P, Lin HG, Wang YY, Tsai CB, Gojon A, Tsay YF (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. Plant Cell 20:2514–2528
López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123
López-Ruiz BA, Zluhan-Martínez E, de la Sánchez PM, Álvarez-Buylla ER, Garay-Arroyo A (2020) interplay between hormones and several abiotic stress conditions on Arabidopsis thaliana primary root development. Cells 9:2576
Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512
Ma T, Wu W, Wang Y (2012) Transcriptome analysis of rice root responses to potassium deficiency. BMC Plant Biol 12:161
Maeda Y, Konishi M, Kiba T, Sakuraba Y, Sawaki N, Kurai T, Ueda Y, Sakakibara H, Yanagisawa S (2018) A NIGT1-centred transcriptional cascade regulates nitrate signalling and incorporates phosphorus starvation signals in Arabidopsis. Nat Commun 9(1):1376
Manoli A, Trevisan S, Quaggiotti S, Varotto S (2018) Identification and characterization of the BZR transcription factor family and its expression in response to abiotic stresses in Zea mays L. Plant Growth Regul 84:423–436
Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant-Microbe Interact 19:1127–1137
Mohanty B, Krishnan SPT, Swarup S, Bajic VB (2005) Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Ann Bot 96:669–681
Naeem M, Khan MMA (2009) Phosphorus ameliorates crop productivity, photosynthesis, nitrate reductase activity and nutrient accumulation in coffee senna (Senna occidentalis L.) under phosphorus-deficient soil. J Plant Interact 4:145–153
Nam YJ, Tran LSP, Kojima M, Sakakibara H, Nishiyama R, Shin R (2012) Regulatory roles of cytokinins and cytokinin signaling in response to potassium deficiency in Arabidopsis. PLoS ONE 7:e47797
Nash J, Luehrsen KR, Walbot V (1990) Bronze-2 gene of maize: reconstruction of a wild-type allele and analysis of transcription and splicing. Plant Cell 2:1039–1049
Nasr Esfahani M, Inoue K, Nguyen KH, Chu HD, Watanabe Y, Kanatani A, Burritt DJ, Mochida K, Tran LSP (2021) Phosphate or nitrate imbalance induces stronger molecular responses than combined nutrient deprivation in roots and leaves of chickpea plants. Plant Cell Environ 44:574–597
Nieves-Cordones M, Ródenas R, Lara A, Martínez V, Rubio F (2019) The combination of K+ deficiency with other environmental stresses: what is the outcome? Physiol Plant 165:264–276
O’Brien JAA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi G, Gutiérrez RAA (2016) Nitrate transport, sensing, and responses in plants. Mol Plant 9:837–856
Oddo E, Inzerillo S, La Bella F, Grisafi F, Salleo S, Nardini A (2011) Short-term effects of potassium fertilization on the hydraulic conductance of Laurus nobilis L. Tree Physiol 31:131–138
Olive MR, Walker JC, Singh K, Dennis ES, Peacock WJ (1990) Functional properties of the anaerobic responsive element of the maize Adh1 gene. Plant Mol Biol 15:593–604
Park JH, Halitschke R, Kim HB, Baldwin IT, Feldmann KA, Feyereisen R (2002) A knock-out mutation in allene oxide synthase results in male sterility and defective wound signal transduction in Arabidopsis due to a block in jasmonic acid biosynthesis. Plant J 31:1–12
Pettigrew WT (2008) Potassium influences on yield and quality production for maize, wheat, soybean and cotton. Physiol Plant 133:670–681
Promchuea S, Zhu Y, Chen Z, Zhang J, Gong Z (2017) ARF2 coordinates with PLETHORAs and PINs to orchestrate ABA-mediated root meristem activity in Arabidopsis. J Integr Plant Biol 59:30–43
Raddatz N, de los Morales RL, Lindahl M, Quintero FJ, Pardo JM (2020) Coordinated transport of nitrate, potassium, and sodium. Front Plant Sci 11:247
Riemann M, Müller A, Korte A, Furuya M, Weiler EW, Nick P (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. Plant Physiol 133:1820–1830
Riemann M, Haga K, Shimizu T et al (2013) Identification of rice allene oxide cyclase mutants and the function of jasmonate for defence against Magnaporthe oryzae. Plant J 74:226–238
Riveras E, Alvarez JM, Vidal EA, Oses C, Vega A, Gutiérrez RA (2015) The calcium ion is a second messenger in the nitrate signaling pathway of Arabidopsis. Plant Physiol 169:1397–1404
Römheld V, Kirkby EA (2010) Research on potassium in agriculture: needs and prospects. Plant Soil 335:155–180
Rouster J, Leah R, Mundy J, Cameron-Mills V (1997) Identification of a methyl jasmonate-responsive region in the promoter of a lipoxygenase 1 gene expressed in barley grain. Plant J 11:513–523
Ruan J, Zhou Y, Zhou M, Yan J, Khurshid M, Weng W, Cheng J, Zhang K (2019) Jasmonic acid signaling pathway in plants. Int J Mol Sci 20(10):2479
Sagar S, Deepika BDK, Chandrasekar R, Singh A (2021) Genome-wide identification, structure analysis and expression profiling of phospholipases D under hormone and abiotic stress treatment in chickpea (Cicer arietinum). Int J Biol Macromol 169:264–273
Sakai T, Takahashi Y, Nagata T (1996) Analysis of the promoter of the auxin-inducible gene, parC, of tobacco. Plant Cell Physiol 37:906–913
Sanders PM, Lee PY, Biesgen C, Boone JD, Beals TP, Weiler EW, Goldberg RB (2000) The Arabidopsis DELAYED DEHISCENCE1 gene encodes an enzyme in the jasmonic acid synthesis pathway. Plant Cell 12:1041–1061
Schachtman DP (2015) The role of ethylene in plant responses to K+ deficiency. Front Plant Sci 6:1153
Schachtman DP, Shin R (2006) Nutrient sensing and signaling: NPKS. Annu Rev Plant Biol 58:47–69
Scheible WR, Rojas-Triana M (2015) Sensing, signaLling, and CONTROL of phosphate starvation in plants: molecular players and applications. Annu Plant Rev 48:23–63
Schmelz EA, Alborn HT, Engelberth J, Tumlinson JH (2003) Nitrogen deficiency increases volicitin-induced volatile emission, jasmonic acid accumulation, and ethylene sensitivity in maize. Plant Physiol 133:295–306
Shin R, Schachtman DP (2004) Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc Natl Acad Sci USA 101:8827–8832
Shin R, Burch AY, Huppert KA, Tiwari SB, Murphy AS, Guilfoyle TJ, Schachtman DP (2007) The Arabidopsis transcription Factor MYB77 modulates auxin signal transduction. Plant Cell 19:2440–2453
Singh A, Pandey GK (2015) Primer design using primer express® for SYBR green-based quantitative PCR. PCR primer design. Humana Press, New York, pp 153–164
Singh A, Baranwal V, Shankar A, Kanwar P et al (2012) Rice phospholipase a superfamily: organization, phylogenetic and expression analysis during abiotic stresses and development. PLoS ONE 7:e30947
Singh AP, Pandey BK, Deveshwar P, Narnoliya L, Parida SK, Giri J (2015) JAZ repressors: potential involvement in nutrients deficiency response in rice and chickpea. Front Plant Sci 6:22–31
Singh M, Singh VP, Prasad SM (2016) Responses of photosynthesis, nitrogen and proline metabolism to salinity stress in Solanum lycopersicum under different levels of nitrogen supplementation. Plant Physiol Biochem 109:72–83
Sinha K, Kaur R, Singh N, Kaur S, Rishi V, Bhunia RK (2020) Mobilization of storage lipid reserve and expression analysis of lipase and lipoxygenase genes in rice (Oryza sativa var Pusa Basmati 1) bran during germination. Phytochemistry 180:112538
Sobajima H, Tani T, Chujo T, Okada K, Suzuki K, Mori S, Minami E, Nishiyama M, Nojiri H, Yamane H (2007) Identification of a jasmonic acid-responsive region in the promoter of the rice 12-oxophytodienoic acid reductase 1 gene OsOPR1. Biosci Biotechnol Biochem 71:3110–3115
Song S, Qi T, Huang H, Ren Q, Wu D, Chang C, Peng W, Liu Y, Peng J, Xie D (2011) The jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23:1000–1013
Song S, Qi T, Huang H, Xie D (2013) Regulation of stamen development by coordinated actions of jasmonate, auxin, and gibberellin in Arabidopsis. Mol Plant 6:1065–1073
Song L, Yu H, Dong J, Che X, Jiao Y, Liu D (2016) The molecular mechanism of ethylene-mediated root hair development induced by phosphate starvation. PLoS Genet 12(7):e1006194
Stenzel I, Hause B, Maucher H, Pitzschke A, Miersch O, Ziegler J, Ryan CA, Wasternack C (2003a) Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato—amplification in wound signalling. Plant J 33:577–589
Stenzel I, Hause B, Miersch O, Kurz T, Maucher H, Weichert H, Ziegler J, Feussner I, Wasternack C (2003b) Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol Biol 51:895–911
Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proc Natl Acad Sci USA 97:10625–10630
Su L, Dai Z, Li S, Xin H (2015a) A novel system for evaluating drought-cold tolerance of grapevines using chlorophyll fluorescence. BMC Plant Biol 15:82
Su Y, Luo W, Lin W, Ma L, Kabir MH (2015b) Model of cation transportation mediated by high-affinity potassium transporters (HKTs) in higher plants. Biol Proced 17:1–13
Svistoonoff S, Creff A, Reymond A et al (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat Genet 39:792–796
Tahir M, Tanv A, Allah AAW (2008) Growth and yield response of two wheat (Triticum aestivum L.) varieties to different potassium levels. Pak J Life Soc Sci 6:92–95
Takatsuka H, Umeda M (2014) Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot 65:2633–2643
Takehisa H, Sato Y, Antonio BA, Nagamur Y (2013) Global transcriptome profile of rice root in response to essential macronutrient deficiency. Plant Signal Behav 8:e24409
Tani T, Sobajima H, Okada K, Chujo T, Arimura SI, Tsutsumi N, Nishimura M, Seto H, Nojiri H, Yamane H (2008) Identification of the OsOPR7 gene encoding 12-oxophytodienoate reductase involved in the biosynthesis of jasmonic acid in rice. Planta 227:517–526
Tariq M, Saeed A, Nisar M, Mian IA, Afzal M (2011) Effect of potassium rates and sources on the growth performance and on chloride accumulation of maize in two different textured soils of Haripur, Hazara division. Sarhad J Agric 27:415–422
Tariq A, Pan K, Olatunji OA, Graciano C, Li Z, Li N, Song D, Sun F, Wu X, Dakhil MA, Sun X, Zhang L (2019) Impact of phosphorus application on drought resistant responses of Eucalyptus grandis seedlings. Physiol Plant 166:894–908
Tran TT, Kano-Nakata M, Takeda M, Menge D, Mitsuya S, Inukai Y, Yamauchi A (2014) Nitrogen application enhanced the expression of developmental plasticity of root systems triggered by mild drought stress in rice. Plant Soil 378:139–152
Villar-Salvador P, Peñuelas JL, Jacobs DF (2013) Nitrogen nutrition and drought hardening exert opposite effects on the stress tolerance of Pinus pinea L. seedlings. Tree Physiol 33:221–232
Vinod KK, Heuer S (2012) Approaches towards nitrogen- and phosphorus-efficient rice. AoB Plants. pls028
Vissenberg K, Claeijs N, Balcerowicz D, Schoenaers S (2020) Hormonal regulation of root hair growth and responses to the environment in Arabidopsis. J Exp Bot 71:2412–2427
Wakuta S, Suzuki E, Saburi W, Matsuura H, Nabeta K, Imai R, Matsui H (2011) OsJAR1 and OsJAR2 are jasmonyl-l-isoleucine synthases involved in wound- and pathogen-induced jasmonic acid signalling. Biochem Biophys Res Commun 409:634–639
Wang Y, Liu GJ, Yan XF, Wei ZG, Xu ZR (2011) MeJA-inducible expression of the heterologous JAZ2 promoter from Arabidopsis in Populus trichocarpa protoplasts. J Plant Dis Prot 118:69–74
Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14:7370–7390
Waraich EA, Ahmad R, Halim A, Aziz T (2012) Alleviation of temperature stress by nutrient management in crop plants: a review. J Soil Sci Plant Nutr 12:221–244
Wasternack C (2015) How jasmonates earned their laurels: past and present. J Plant Growth Regul 34:761–794
Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321
Wasternack C, Strnad M (2018) Jasmonates: news on occurrence, biosynthesis, metabolism and action of an ancient group of signaling compounds. Int J Mol Sci 19(9):2539
White AJ, Alison Dunn M, Brown K, Hughes MA (1994) Comparative analysis of genomic sequence and expression of a lipid transfer protein gene family in winter barley. J Exp Bot 45:1885–1892
Wissuwa M, Kretzschmar T, Rose TJ (2016) From promise to application: root traits for enhanced nutrient capture in rice breeding. J Exp Bot 67:3605–3615
Xiao Y, Chen Y, Charnikhova T et al (2014) OsJAR1 is required for JA-regulated floret opening and anther dehiscence in rice. Plant Mol Biol 86:19–33
Xing H, Pudake RN, Guo G, Xing G, Hu Z, Zhang Y, Sun Q, Ni Z (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genom 12:178
Xu J, Li HD, Chen LQ, Wang Y, Liu LL, He L, Wu WH (2006) A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis. Cell 125:1347–1360
Yan Y, Borrego E, Kolomiets MV (2013) Jasmonate biosynthesis, perception and function in plant development and stress responses. Lipid Metab. InTech, pp 393–442
Yang N, Zhu C, Gan L, Ng D, Xia K (2011) Ammonium-stimulated root hair branching is enhanced by methyl jasmonate and suppressed by ethylene in Arabidopsis thaliana. J Plant Biol 54:92–100
Yang L, Zhang J, He J, Qin Y, Hua D, Duan Y, Chen Z, Gong Z (2014) ABA-mediated ROS in mitochondria regulate root meristem activity by controlling PLETHORA expression in Arabidopsis. PLoS Genet 10(12):e1004791
Yu C, Chen Y, Lu C, Hwang J (2006) Prediction of protein subcellular localization. Proteins Struct Funct Bioinforma 64:643–651
Zain NA, Ismail MR, Puteh A, Mahmood M, Islam MR (2014) Drought tolerance and ion accumulation of rice following application of additional potassium fertilizer. Commun Soil Sci Plant Anal 45:2502–2514
Zhang H, Han W, De Smet I, Talboys P, Loya R, Hassan A, Rong H, Jürgens G, Paul Knox J, Wang MH (2010) ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem. Plant J 64:764–774
Zhang G, Yi HY, Gong JM (2014) The Arabidopsis ethylene/jasmonic acid-NRT signaling module coordinates nitrate reallocation and the trade-off between growth and environmental adaptation. Plant Cell 26:3984–3998
Zhang Y, Tan L, Zhu Z, Yuan L, Xie D, Sun C (2015) TOND1 confers tolerance to nitrogen deficiency in rice. Plant J 81:367–376
Zhang X, Jiang H, Wang H, Cui J, Wang J, Hu J, Guo L, Qian Q, Xue D (2017) Transcriptome analysis of rice seedling roots in response to potassium deficiency. Sci Rep 7(1):5523
Zhao C, Liu Q (2009) Growth and physiological responses of Picea asperata seedlings to elevated temperature and to nitrogen fertilization. Acta Physiol Plant 31:163–173
Zheng H, Pan X, Deng Y, Wu H, Liu P, Li X (2016) AtOPR3 specifically inhibits primary root growth in Arabidopsis under phosphate deficiency. Sci Rep 6:24778
Zhong C, Cao X, Hu J, Zhu L, Zhang J, Huang J, Jin Q (2017) Nitrogen metabolism in adaptation of photosynthesis to water stress in rice grown under different nitrogen levels. Front Plant Sci 8:1079
Zhou W, Lozano-Torres JL, Blilou I, Zhang X, Zhai Q, Smant G, Li C, Scheres B (2019) A jasmonate signaling network activates root stem cells and promotes regeneration. Cell 177:942–956
Zhu Z, An F, Feng Y et al (2011) Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc Natl Acad Sci USA 108:12539–12544
Acknowledgements
Authors are thankful to DBT (Department of Biotechnology)- eLibrary Consortium (DeLCON) for providing e-resources and National Institute of Plant Genome Research (NIPGR) for financial support from core research grant. Deepika acknowledges council of scientific and industrial research (CSIR), India for research fellowships.
Funding
Research fund was provided by the National Institute of Plant Genome Research (NIPGR), India core research grant.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Authors declare that there is no conflict of interests.
Additional information
Communicated by Aryadeep Roychoudhury.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Deepika, Singh, A. Expression dynamics indicate the role of Jasmonic acid biosynthesis pathway in regulating macronutrient (N, P and K+) deficiency tolerance in rice (Oryza sativa L.). Plant Cell Rep 40, 1495–1512 (2021). https://doi.org/10.1007/s00299-021-02721-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-021-02721-5