Nitrate increases ethylene production and aerenchyma formation in roots of lowland rice plants under water stress
Cuimin Gao A B * , Lei Ding A * , Yingrui Li A , Yupei Chen A , Jingwen Zhu A , Mian Gu A , Yong Li C , Guohua Xu A , Qirong Shen A and Shiwei Guo A D
+ Author Affiliations
- Author Affiliations
A College of Resources and Environmental Sciences, Nanjing Agricultural University, National Engineering Research Center for Organic-based Fertilizers, Nanjing 210095, China.
B Institute of Plant Nutrition, Agricultural Resources and Environmental Sciences, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China.
C Crop Physiology and Production Center, Huazhong Agricultural University, Wuhan, Hubei 430070, China.
D Corresponding author. Email: sguo@njau.edu.cn
Functional Plant Biology 44(4) 430-442 https://doi.org/10.1071/FP16258
Submitted: 7 January 2016 Accepted: 9 December 2016 Published: 31 January 2017
Abstract
Ethylene increases root cortical aerenchyma formation in maize (Zea mays L.), rice (Oryza sativa L.) and other species. To further investigate the effects of nitrate, ammonium and water stress on ethylene production and aerenchyma formation in roots, two lowland rice cultivars (Shanyou 63, hybrid indica, and Yangdao 6, inbred indica) were cultured hydroponically with 10% (w/v) polyethylene glycol to simulate water stress. Water stress decreased shoot biomass, stomatal conductivity and leaf water potential in cultivars fed with nitrate but not with ammonium. Water stress induced more aerenchyma formation in cultivars fed with nitrate rather than ammonium, and increased cortical aerenchyma was found in Yangdao 6. Endogenous ethylene production by roots increased significantly under water stress in plants fed with nitrate rather than ammonium. Exogenous ethylene stimulated root cortical aerenchyma formation. Expression of the ethylene biosynthesis gene 1-aminocyclo-propane-1-carboxylic acid (ACC) synthase (ACS5) was greater in roots fed with nitrate rather than ammonium in the presence and absence of water stress. The expression of ethylene signalling pathway genes involved in programmed cell death (lesion-simulating disease (L.S.D.)1.1 and L.S.D.2; enhanced disease susceptibility (EDS) and phytoalexin-deficient (PAD4)) were regulated by the N form and water stress. In plants of cultivars fed with ammonium, L.S.D.1.1 expression increased under water stress, whereas L.S.D.2, EDS and PAD4 expression decreased. In conclusion, nitrate increases ethylene production and cortical aerenchyma formation in roots of water-stressed lowland rice. However, ammonium increased L.S.D.1.1 expression in water-stressed roots, and decreased ACS5, EDS and PAD4 expression, which would inhibit ethylene production and aerenchyma formation.
Additional keywords: ethylene signalling pathway genes, gene expression, nitrogen form, Oryza sativa.
References
Barry CS, Llop-Tous MI, Grierson D (2000) The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato. Plant Physiology 123, 979–986.| The regulation of 1-aminocyclopropane-1-carboxylic acid synthase gene expression during the transition from system-1 to system-2 ethylene synthesis in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1Sltrw%3D&md5=9550f0fb24baa87068e9ab172e814801CAS |
Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytologist 162, 671–681.
| Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltlyrsro%3D&md5=541ef2db07f55e0aa022aba2cc83df58CAS |
Bragina T, Martinovich L, Rodionova N, Bezborodov A, Grineva G (2001) Ethylene-induced activation of xylanase in adventitious roots of maize as a response to the stress effect of root submersion. Applied Biochemistry and Microbiology 37, 618–621.
| Ethylene-induced activation of xylanase in adventitious roots of maize as a response to the stress effect of root submersion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXosVGhu7c%3D&md5=a22c17526154b41bda9cf9e039695830CAS |
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 Science 234, 14–21.
| The enhanced drought tolerance of rice plants under ammonium is related to aquaporin (AQP).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXisl2qs7g%3D&md5=16763e5bee8efa4704d77d18d9d3e654CAS |
Drew M, Jackson M, Giffard S (1979) Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L. Planta 147, 83–88.
| Ethylene-promoted adventitious rooting and development of cortical air spaces (aerenchyma) in roots may be adaptive responses to flooding in Zea mays L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtVOmtbc%3D&md5=b8324fa7885208409ac95c2c3b82de8aCAS |
Drew MC, Jackson MB, Giffard SC, Campbell R (1981) Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency. Planta 153, 217–224.
| Inhibition by silver ions of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to exogenous ethylene or to oxygen deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL38XjvFak&md5=f5b89d4b61b98c8f10f681d68f5b5a12CAS |
Duan Y, Zhang W, Li B, Wang Y, Li K, Sodmergen , Han C, Zhang Y, Li X (2010) An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis. New Phytologist 186, 681–695.
| An endoplasmic reticulum response pathway mediates programmed cell death of root tip induced by water stress in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsVejt7g%3D&md5=7c6d50491d9c51e90ad61c69027cfdc0CAS |
Evans DE (2004) Aerenchyma formation. New Phytologist 161, 35–49.
| Aerenchyma formation.Crossref | GoogleScholarGoogle Scholar |
Fan M, Zhu J, Richards C, Brown KM, Lynch JP (2003) Physiological roles for aerenchyma in phosphorus-stressed roots. Functional Plant Biology 30, 493–506.
| Physiological roles for aerenchyma in phosphorus-stressed roots.Crossref | GoogleScholarGoogle Scholar |
Gao YX, Li Y, Yang XX, Li HJ, Shen QR, Guo SW (2010) Ammonium nutrition increases water absorption in rice seedlings (Oryza sativa L.) under water stress. Plant and Soil 331, 193–201.
| Ammonium nutrition increases water absorption in rice seedlings (Oryza sativa L.) under water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvVOhsbo%3D&md5=df3b3a48eb3ce67118f8a896e34b4375CAS |
Godfray HC, Beddington JR, Crute IR, Haddad L, Lawrence D, Muir JF, Pretty J, Robinson S, Thomas SM, Toulmin C (2010) Food security: the challenge of feeding 9 billion people. Science 327, 812–818.
| Food security: the challenge of feeding 9 billion people.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslWisLo%3D&md5=20663bbe84ccd812a1b89f000eec0701CAS |
Grondin A, Mauleon R, Vadez V, Henry A (2016) Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.). Plant, Cell & Environment 39, 347–365.
| Root aquaporins contribute to whole plant water fluxes under drought stress in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XisVyisLo%3D&md5=a08c24f5b314996e2b54a29cfbc138bdCAS |
Gunawardena AHLAN, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212, 205–214.
| Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjs1Kkuw%3D%3D&md5=5f768ecc24a2f078678a335d78330e49CAS |
Guo S, Zhou Y, Shen Q, Zhang F (2007a) Effect of ammonium and nitrate nutrition on some physiological processes in higher plants – growth, photosynthesis, photorespiration, and water relations. Plant Biology 9, 21–29.
| Effect of ammonium and nitrate nutrition on some physiological processes in higher plants – growth, photosynthesis, photorespiration, and water relations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXivF2gsLw%3D&md5=e6a9bfba395acbc4909f73da27979233CAS |
Guo SW, Chen G, Zhou Y, Shen QR (2007b) Ammonium nutrition increases photosynthesis rate under water stress at early development stage of rice (Oryza sativa L.). Plant and Soil 296, 115–124.
| Ammonium nutrition increases photosynthesis rate under water stress at early development stage of rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnsFejs74%3D&md5=6b156aa3cc017c1c197e2c335ed4f969CAS |
Guo S, Zhou Y, Li Y, Gao Y, Shen Q (2008) Effects of different nitrogen forms and osmotic stress on water use efficiency of rice (Oryza sativa). Annals of Applied Biology 153, 127–134.
| Effects of different nitrogen forms and osmotic stress on water use efficiency of rice (Oryza sativa).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWmsrzN&md5=342f9f55b838ed3975258622e9118b03CAS |
Henry A, Cal AJ, Batoto TC, Torres RO, Serraj R (2012) Root attributes affecting water uptake of rice (Oryza sativa) under drought. Journal of Experimental Botany 63, 4751–4763.
| Root attributes affecting water uptake of rice (Oryza sativa) under drought.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1KjsLbI&md5=50b58c582e746d5b0e1d5d04d8e3bc70CAS |
Hu J, Zhou JB, Peng XX, Xu HH, Liu CX, Du B, Yuan HY, Zhu LL, He GC (2011) The Bphi008a gene interacts with the ethylene pathway and transcriptionally regulates MAPK genes in the response of rice to brown planthopper feeding. Plant Physiology 156, 856–872.
| The Bphi008a gene interacts with the ethylene pathway and transcriptionally regulates MAPK genes in the response of rice to brown planthopper feeding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnvFWrtrc%3D&md5=6d32b49a156a865150bbbfb4f0e46b9bCAS |
Iqbal N, Nazar R, Syeed S, Masood A, Khan NA (2011) Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard. Journal of Experimental Botany 62, 4955–4963.
| Exogenously-sourced ethylene increases stomatal conductance, photosynthesis, and growth under optimal and deficient nitrogen fertilization in mustard.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlejsrfJ&md5=d0533e5b165379a98668dc4510c989c8CAS |
Jackson MB (1985) Ethylene and responses of plants to soil waterlogging and submergence. Annual Review of Plant Physiology and Plant Molecular Biology 36, 145–174.
| Ethylene and responses of plants to soil waterlogging and submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktlCrtr8%3D&md5=e4f9aafc666d25c60ec2a00c5b3f6671CAS |
Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1, 274–287.
| Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVKjsbk%3D&md5=bea44914619ffb4d82b5bff13feb1600CAS |
Jongdee B, Fukai S, Cooper M (2002) Leaf water potential and osmotic adjustment as physiological traits to improve drought tolerance in rice. Field Crops Research 76, 153–163.
| Leaf water potential and osmotic adjustment as physiological traits to improve drought tolerance in rice.Crossref | GoogleScholarGoogle Scholar |
Joshi R, Kumar P (2012) Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots. Physiology and Molecular Biology of Plants 18, 1–9.
| Lysigenous aerenchyma formation involves non-apoptotic programmed cell death in rice (Oryza sativa L.) roots.Crossref | GoogleScholarGoogle Scholar |
Justin SHFW, Armstrong W (1991) Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza-sativa L). New Phytologist 118, 49–62.
| Evidence for the involvement of ethene in aerenchyma formation in adventitious roots of rice (Oryza-sativa L).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXlsFGit7g%3D&md5=9cca083006d67d8f13dbbf70d9e035a3CAS |
Kim HJ, Lynch JP, Brown KM (2008) Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant, Cell & Environment 31, 1744–1755.
| Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXmt1yrug%3D%3D&md5=eba5c9fc1e44c9d472000cfefb6b1c13CAS |
Kohler M, Haerdi W, Christen P, Veuthey J-L (1997) Extraction of artemisinin and artemisinic acid from Artemisia annua L. using supercritical carbon dioxide. Journal of Chromatography. A 785, 353–360.
| Extraction of artemisinin and artemisinic acid from Artemisia annua L. using supercritical carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmsVKkt7o%3D&md5=430a2d1db748224c01d80f9af59af834CAS |
Konings H, Verschuren G (1980) Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply. Physiologia Plantarum 49, 265–270.
| Formation of aerenchyma in roots of Zea mays in aerated solutions, and its relation to nutrient supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXltFeisLo%3D&md5=0ba001f238b9218a42abd9cf861694cbCAS |
Leon-Reyes A, Du Y, Koornneef A, Proietti S, Körbes AP, Memelink J, Pieterse CM, Ritsema T (2010) Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid. Molecular Plant-Microbe Interactions 23, 187–197.
| Ethylene signaling renders the jasmonate response of Arabidopsis insensitive to future suppression by salicylic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXovVWktg%3D%3D&md5=1869d34879bdda93e7bb0a39fd29cf9aCAS |
Li Y-S, Mao X-T, Tian Q-Y, Li L-H, Zhang W-H (2009a) Phosphorus deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production. Environmental and Experimental Botany 67, 172–177.
| Phosphorus deficiency-induced reduction in root hydraulic conductivity in Medicago falcata is associated with ethylene production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtV2qs7rF&md5=b1557fac89586e938cce4b6140c89514CAS |
Li Y, Gao YX, Ding L, Shen QR, Guo SW (2009b) Ammonium enhances the tolerance of rice seedlings (Oryza sativa L.) to drought condition. Agricultural Water Management 96, 1746–1750.
| Ammonium enhances the tolerance of rice seedlings (Oryza sativa L.) to drought condition.Crossref | GoogleScholarGoogle Scholar |
Li Y, Ren BB, Yang XX, Xu GH, Shen QR, Guo SW (2012) Chloroplast downsizing under nitrate nutrition restrained mesophyll conductance and photosynthesis in rice (Oryza sativa L.) under drought conditions. Plant & Cell Physiology 53, 892–900.
| Chloroplast downsizing under nitrate nutrition restrained mesophyll conductance and photosynthesis in rice (Oryza sativa L.) under drought conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntVSjsLw%3D&md5=eb5e02aa15cdd9613bbf9b954b345145CAS |
Liao CT, Lin CH (2001) Physiological adaptation of crop plants to flooding stress. Proceedings of the National Science Council, Republic of China. Part B, Life Sciences 25, 148–157.
Mateo A, Mühlenbock P, Rustérucci C, Chang CC-C, Miszalski Z, Karpinska B, Parker JE, Mullineaux PM, Karpinski S (2004) LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy. Plant Physiology 136, 2818–2830.
| LESION SIMULATING DISEASE 1 is required for acclimation to conditions that promote excess excitation energy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOqsrk%3D&md5=9c0c3a15d8c2f8f15c549103a11092a0CAS |
Mathooko FM, Inaba A, Nakamura R (1998) Characterization of carbon dioxide stress-induced ethylene biosynthesis in cucumber (Cucumis sativus L.) fruit. Plant & Cell Physiology 39, 285–293.
| Characterization of carbon dioxide stress-induced ethylene biosynthesis in cucumber (Cucumis sativus L.) fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXitVWmt7o%3D&md5=69c5e6954340c7b1bb4904d78d4c9774CAS |
Michel BE, Kaufmann MR (1973) The osmotic potential of polyethylene glycol 6000. Plant Physiology 51, 914–916.
| The osmotic potential of polyethylene glycol 6000.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3sXktVGkt7o%3D&md5=8f8a3f4f5efe8ab133663a9a71294482CAS |
Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjarvi J (2002) Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato. Plant Physiology 130, 1918–1926.
| Ethylene synthesis regulated by biphasic induction of 1-aminocyclopropane-1-carboxylic acid synthase and 1-aminocyclopropane-1-carboxylic acid oxidase genes is required for hydrogen peroxide accumulation and cell death in ozone-exposed tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktlKh&md5=3ae526e97c53bca8b915fa12677fb67cCAS |
Mühlenbock P, Plaszczyca M, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1. The Plant Cell 19, 3819–3830.
| Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1.Crossref | GoogleScholarGoogle Scholar |
Mühlenbock P, Szechyńska-Hebda M, Płaszczyca M, Baudo M, Mateo A, Mullineaux PM, Parker JE, Karpińska B, Karpiński S (2008) Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis. The Plant Cell 20, 2339–2356.
| Chloroplast signaling and LESION SIMULATING DISEASE1 regulate crosstalk between light acclimation and immunity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Niones JM, Suralta RR, Inukai Y, Yamauchi A (2013) Roles of root aerenchyma development and its associated QTL in dry matter production under transient moisture stress in rice. Plant Production Science 16, 205–216.
| Roles of root aerenchyma development and its associated QTL in dry matter production under transient moisture stress in rice.Crossref | GoogleScholarGoogle Scholar |
Parent B, Suard B, Serraj R, Tardieu F (2010) Rice leaf growth and water potential are resilient to evaporative demand and soil water deficit once the effects of root system are neutralized. Plant, Cell & Environment 33, 1256–1267.
Postma JA, Lynch JP (2011) Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiology 156, 1190–1201.
| Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWksr4%3D&md5=e1c269f60b276d64f485ea2348a66a0bCAS |
Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytologist 190, 351–368.
| Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmt1GktLc%3D&md5=7a2c0b02efddf66f4b1cda907406b873CAS |
Ranathunge K, Kotula L, Steudle E, Lafitte R (2004) Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. Journal of Experimental Botany 55, 433–447.
| Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXms1entQ%3D%3D&md5=b686ce6fd0325fa39469bd4d8d947c64CAS |
Ray DK, Mueller ND, West PC, Foley JA (2013) Yield trends are insufficient to double global crop production by 2050. PLoS One 8,
| Yield trends are insufficient to double global crop production by 2050.Crossref | GoogleScholarGoogle Scholar |
Rustérucci C, Aviv DH, Holt BF, Dangl JL, Parker JE (2001) The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis. The Plant Cell 13, 2211–2224.
| The disease resistance signaling components EDS1 and PAD4 are essential regulators of the cell death pathway controlled by LSD1 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Sharp RE, LeNoble ME (2002) ABA, ethylene and the control of shoot and root growth under water stress. Journal of Experimental Botany 53, 33–37.
| ABA, ethylene and the control of shoot and root growth under water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXptlKgtLs%3D&md5=eeb03e6a0c58f418a77785ff46170e69CAS |
Stitt M (1999) Nitrate regulation of metabolism and growth. Current Opinion in Plant Biology 2, 178–186.
| Nitrate regulation of metabolism and growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXkt1Cgs7w%3D&md5=3a813a2d9c548a46949b36d7df6c7be8CAS |
Suralta RR, Yamauchi A (2008) Root growth, aerenchyma development, and oxygen transport in rice genotypes subjected to drought and waterlogging. Environmental and Experimental Botany 64, 75–82.
| Root growth, aerenchyma development, and oxygen transport in rice genotypes subjected to drought and waterlogging.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpvF2qtrs%3D&md5=cc0bb4e1373b01e4b73a5d348e058b23CAS |
Tomishige K, Furusawa Y, Ikeda Y, Asadullah M, Fujimoto K (2001) CeO2–ZrO2 solid solution catalyst for selective synthesis of dimethyl carbonate from methanol and carbon dioxide. Catalysis Letters 76, 71–74.
| CeO2–ZrO2 solid solution catalyst for selective synthesis of dimethyl carbonate from methanol and carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovVemsr8%3D&md5=8b18c76aaf12c83fac95678789b0a864CAS |
Turner N, Long M (1980) Errors arising from rapid water loss in the measurement of leaf water potential by the pressure chamber technique. Functional Plant Biology 7, 527–537.
Verslues PE, Ober ES, Sharp RE (1998) Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions. Plant Physiology 116, 1403–1412.
| Root growth and oxygen relations at low water potentials. Impact of oxygen availability in polyethylene glycol solutions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisFyqtrw%3D&md5=0b3d9c4db84f6dd75aeef3467bb17f88CAS |
Wang L, Pei Z, Tian Y, He C (2005) OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation. Molecular Plant—Microbe Interactions 18, 375–384.
| OsLSD1, a rice zinc finger protein, regulates programmed cell death and callus differentiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjslams7s%3D&md5=2c64c570ace467f6f38dce6e03bf90d0CAS |
Williams L, Araujo F (2002) Correlations among predawn leaf, midday leaf, and midday stem water potential and their correlations with other measures of soil and plant water status in Vitis vinifera. Journal of the American Society for Horticultural Science 127, 448–454.
Wituszyńska W, Ślesak I, Vanderauwera S, Szechyńska-Hebda M, Kornaś A, Van Der Kelen K, Mühlenbock P, Karpińska B, Maćkowski S, Van Breusegem F (2013) LESION SIMULATING DISEASE1, ENHANCED DISEASE SUSCEPTIBILITY1, and PHYTOALEXIN DEFICIENT4 conditionally regulate cellular signaling homeostasis, photosynthesis, water use efficiency, and seed yield in Arabidopsis. Plant Physiology 161, 1795–1805.
| LESION SIMULATING DISEASE1, ENHANCED DISEASE SUSCEPTIBILITY1, and PHYTOALEXIN DEFICIENT4 conditionally regulate cellular signaling homeostasis, photosynthesis, water use efficiency, and seed yield in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Wu C, Ye Z, Shu W, Zhu Y, Wong M (2011) Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes. Journal of Experimental Botany 62, 2889–2898.
| Arsenic accumulation and speciation in rice are affected by root aeration and variation of genotypes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmsVyksLY%3D&md5=5ac8f2c0d1617be81f35aad6ce644cfaCAS |
Wu J, Zhu C, Pang J, Zhang X, Yang C, Xia G, Tian Y, He C (2014) OsLOL1, a C2C2‐type zinc finger protein, interacts with OsbZIP58 to promote seed germination through the modulation of gibberellin biosynthesis in Oryza sativa. The Plant Journal 80, 1118–1130.
| OsLOL1, a C2C2‐type zinc finger protein, interacts with OsbZIP58 to promote seed germination through the modulation of gibberellin biosynthesis in Oryza sativa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXitVOhtbbL&md5=0b9a9e9a05bd9f40e0c20e04834009adCAS |
Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2014) Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. Journal of Experimental Botany 65, 261–273.
| Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlvF2jtw%3D%3D&md5=6cb7136ebbf17832302e235a2d0a6452CAS |
Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiology 127, 315–323.
| Hormonal changes in the grains of rice subjected to water stress during grain filling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmvFCrtb8%3D&md5=249bf7f437a9d9927977dff2eedb68c3CAS |
Yang XX, Li Y, Ren BB, Ding L, Gao CM, Shen QR, Guo SW (2012) Drought-induced root aerenchyma formation restricts water uptake in rice seedlings supplied with nitrate. Plant & Cell Physiology 53, 495–504.
| Drought-induced root aerenchyma formation restricts water uptake in rice seedlings supplied with nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjslehu70%3D&md5=68667ad8554d341c11300bccfde68f43CAS |
Yin DM, Chen SM, Chen FD, Jiang JF (2013) Ethylene promotes induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema spp. Molecular Biology Reports 40, 4581–4590.
| Ethylene promotes induction of aerenchyma formation and ethanolic fermentation in waterlogged roots of Dendranthema spp.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXps1Cmtrg%3D&md5=b18acf73bf331aabb27616ff7ed214deCAS |
Yu K, Zhong W, Yunjie G, Fei X, Gang C, Ying H (2009) Induction of ethephon on aerenchyma formation in rice roots. Chinese Journal of Rice Science 23, 65–70.
Zhu J, Liang J, Xu Z, Fan X, Zhou Q, Shen Q, Xu G (2015) Root aeration improves growth and nitrogen accumulation in rice seedlings under low nitrogen. AoB Plants 7, plv131
| Root aeration improves growth and nitrogen accumulation in rice seedlings under low nitrogen.Crossref | GoogleScholarGoogle Scholar |
