Molecular insights into the functional role of nitric oxide (NO) as a signal for plant responses in chickpea
Parankusam Santisree A B , Pooja Bhatnagar-Mathur A and Kiran K. Sharma A
+ Author Affiliations
- Author Affiliations
A International Crops Research Institute for the Semiarid Tropics (ICRISAT), Patancheru, Hyderabad-502324, Telangana, India.
B Corresponding authors. Email: s.parankusam@cgiar.org; santhikinnu@gmail.com
Functional Plant Biology 45(2) 267-283 https://doi.org/10.1071/FP16324
Submitted: 20 September 2016 Accepted: 14 March 2017 Published: 13 April 2017
Abstract
The molecular mechanisms and targets of nitric oxide (NO) are not fully known in plants. Our study reports the first large-scale quantitative proteomic analysis of NO donor responsive proteins in chickpea. Dose response studies carried out using NO donors, sodium nitroprusside (SNP), diethylamine NONOate (DETA) and S-nitrosoglutathione (GSNO) in chickpea genotype ICCV1882, revealed a dose dependent positive impact on seed germination and seedling growth. SNP at 0.1 mM concentration proved to be most appropriate following confirmation using four different chickpea genotypes. while SNP treatment enhanced the percentage of germination, chlorophyll and nitrogen contents in chickpea, addition of NO scavenger, cPTIO reverted its impact under abiotic stresses. Proteome profiling revealed 172 downregulated and 76 upregulated proteins, of which majority were involved in metabolic processes (118) by virtue of their catalytic (145) and binding (106) activity. A few crucial proteins such as S-adenosylmethionine synthase, dehydroascorbate reductase, pyruvate kinase fragment, 1-aminocyclopropane-1-carboxylic acid oxidase, 1-pyrroline-5-carboxylate synthetase were less abundant whereas Bowman-Birk type protease inhibitor, non-specific lipid transfer protein, chalcone synthase, ribulose-1-5-bisphosphate carboxylase oxygenase large subunit, PSII D2 protein were highly abundant in SNP treated samples. This study highlights the protein networks for a better understanding of possible NO induced regulatory mechanisms in plants.
Additional keywords: abiotic stress, gel-free proteomics, mass spectroscopy, sodium nitroprusside.
References
Anbazhagan K, Bhatnagar-Mathur P, Vadez V, Dumbala SR, Kishor PBK, Sharma KK (2015) DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes. Plant Cell Reports 34, 199–210.| DREB1A overexpression in transgenic chickpea alters key traits influencing plant water budget across water regimes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsl2lsrrI&md5=820b033b398c529640ba0f0ff05bd387CAS |
Astier J, Lindermayr C (2012) Nitric oxide-dependent posttranslational modification in plants: an update. International Journal of Molecular Sciences 13, 15193–15208.
| Nitric oxide-dependent posttranslational modification in plants: an update.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVequrrO&md5=8579ccf3004e44066309462a01f8864eCAS |
Bai X, Yang L, Yang Y, Ahmad P, Yang Y, Hu X (2011) Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize. Journal of Proteome Research 10, 4349–4364.
| Deciphering the protective role of nitric oxide against salt stress at the physiological and proteomic levels in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFeiurbK&md5=73f9384b646af9ab6f2ff38e7fce7188CAS |
Barkla BJ, Vera-Estrella R, Pantoja O (2013) Progress and challenges for abiotic stress proteomics of crop plants. Proteomics 13, 1801–1815.
| Progress and challenges for abiotic stress proteomics of crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVGrtbzI&md5=20c5d6833de5e399c6d8d4903d98c096CAS |
Bavita A, Shashi B, Navtej SV (2012) Nitric oxide alleviates oxidative damage induced by high temperature stress in wheat. Indian Journal of Experimental Biology 50, 372–378.
Begara-Morales JC, Sánchez-Calvo B, Luque F, Leyva-Pérez MO, Leterrier M, Corpas FJ, Barroso JB (2014) Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves. Plant & Cell Physiology 55, 1080–1095.
| Differential transcriptomic analysis by RNA-Seq of GSNO-responsive genes between Arabidopsis roots and leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXpvFCrs78%3D&md5=9d07b4d3f013e05f0f757682e326d137CAS |
Beligni MV, Lamattina L (1999) Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants. Nitric Oxide 3, 199–208.
| Nitric oxide protects against cellular damage produced by methylviologen herbicides in potato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXktVSluro%3D&md5=e98291e0cc3d1ca3f942fd4af689169aCAS |
Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210, 215–221.
| Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVWqtg%3D%3D&md5=57a8c9c2e867044e8631b621b10fc2d8CAS |
Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiology 129, 1642–1650.
| Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gtrs%3D&md5=fef6f73a2ab42297928a1618b5631118CAS |
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society. Series B (Methodological) 57, 289–300.
Besson-Bard A, Astier J, Rasul S, Wawer I, Dubreuil-Maurizi C, Jeandroz S, Wendehenne D (2009) Current view of nitric oxide-responsive genes in plants. Plant Science 177, 302–309.
| Current view of nitric oxide-responsive genes in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpt1Kgs78%3D&md5=7a634aff9b5ef8011f70156a116d707aCAS |
Chohan A, Parmar U, Raina SK (2012) Effect of sodium nitroprusside on morphological characters under chilling stress in chickpea (Cicer arietinum L.). Journal of Environmental Biology 33, 695–698.
D’Alessandro S, Posocco B, Costa A, Zahariou G, Lo Schiavo F, Carbonera D, Zottini M (2013) Limits in the use of cPTIO as nitric oxide scavenger and EPR probe in plant cells and seedlings. Frontiers in Plant Science 4, 340
Esim N, Atici O (2013) Nitric oxide alleviates boron toxicity by reducing oxidative damage and growth inhibition in maize seedlings (Zea mays L.). Australian Journal of Crop Science 7, 1085–1092.
Fan H, Li T, Guan L, Li Z, Guo N, Cai Y, Lin Y (2012) Effects of exogenous nitric oxide on antioxidation and DNA methylation of Dendrobium huoshanense grown under drought stress. Plant Cell, Tissue and Organ Culture 109, 307–314.
| Effects of exogenous nitric oxide on antioxidation and DNA methylation of Dendrobium huoshanense grown under drought stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xlt1Slt78%3D&md5=89db044daa94bca4bff2a012d8cec926CAS |
Fan S, Meng Y, Song M, Pang C, Wei H, Liu J, Zhan X, Lan J, Feng C, Zhang S, Yu S (2014) Quantitative phosphoproteomics analysis of nitric oxide–responsive phosphoproteins in cotton leaf. PLoS One 9, e94261
| Quantitative phosphoproteomics analysis of nitric oxide–responsive phosphoproteins in cotton leaf.Crossref | GoogleScholarGoogle Scholar |
Farooq M, Basra MA, Wahid A, Rehman H (2009) Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.). Journal Agronomy & Crop Science 195, 254–261.
| Exogenously applied nitric oxide enhances the drought tolerance in fine grain aromatic rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGit73K&md5=fe84cd16e9e8805745ca80675984bbbeCAS |
Fercha A, Capriotti AL, Caruso G, Cavaliere C, Gherroucha H, Samperi R, Stampachiacchiere S, Lagana A (2013) Gel-free proteomics reveal potential biomarkers of priming-induced salt tolerance in durum wheat. Journal of Proteomics 91, 486–499.
| Gel-free proteomics reveal potential biomarkers of priming-induced salt tolerance in durum wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslClsrbE&md5=034c1bf39b596ff0b74d1dcc9a074386CAS |
Garcia-Mata C, Lamattina L (2001) Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress. Plant Physiology 126, 1196–1204.
| Nitric oxide induces stomatal closure and enhances the adaptive plant responses against drought stress.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3Mvgs1GksA%3D%3D&md5=69c212e76399a7e606ba5a4f7f6a9205CAS |
Groß F, Durner J, Gaupels F (2013) Nitric oxide, antioxidants and prooxidants in plant defence responses. Frontiers in Plant Science 4, 419
| Nitric oxide, antioxidants and prooxidants in plant defence responses.Crossref | GoogleScholarGoogle Scholar |
Gupta R, Wang Y, Agrawal GK, Rakwal R, Jo IH, Bang KH, Kim ST (2015) Time to dig deep into the plant proteome: a hunt for low-abundance proteins. Frontiers in Plant Science 6, 22
| Time to dig deep into the plant proteome: a hunt for low-abundance proteins.Crossref | GoogleScholarGoogle Scholar |
Hayat S, Yadav S, Wani AS, Irfan M, Ahmad A (2011) Nitric oxide effects on photosynthetic rate, growth, and antioxidant activity in tomato. International Journal of Vegetable Science 17, 333–348.
| Nitric oxide effects on photosynthetic rate, growth, and antioxidant activity in tomato.Crossref | GoogleScholarGoogle Scholar |
He Y, Tang RH, Hao Y, Stevens RD, Cook CW, Ahn SM, Jing L, Yang Z, Chen L, Guo F, Fiorani F, Jackson RB, Crawford NM, Pei ZM (2004) Nitric oxide represses the Arabidopsis floral transition. Science 305, 1968–1971.
| Nitric oxide represses the Arabidopsis floral transition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslSlsrg%3D&md5=7b856aaf7512f0f4ab588c901e3c2b0dCAS |
Jasid S, Simontacchi M, Bartoli CG, Puntarulo S (2006) Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins. Plant Physiology 142, 1246–1255.
| Chloroplasts as a nitric oxide cellular source. Effect of reactive nitrogen species on chloroplastic lipids and proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1eju77F&md5=96b286a9a51685bc857a817bcac3d1ddCAS |
Jukanti AK, Gaur PM, Gowda CLL, Chibbar RN (2012) Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review. British Journal of Nutrition 108, S11–S26.
| Nutritional quality and health benefits of chickpea (Cicer arietinum L.): a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1GjurbK&md5=140eb87ef10abe7f751d7e6221cd479cCAS |
Julián I, Gandullo J, Santos-Silva LK, Diaz I, Martinez M (2013) Phylogenetically distant barley legumains have a role in both seed and vegetative tissues. Journal of Experimental Botany 64, 2929–2941.
| Phylogenetically distant barley legumains have a role in both seed and vegetative tissues.Crossref | GoogleScholarGoogle Scholar |
Kaur G, Singh HP, Batish DR, Mahajan P, Kohli RK, Rishi V (2015) Exogenous nitric oxide (NO) interferes with lead (Pb)-induced toxicity by detoxifying reactive oxygen species in hydroponically grown wheat (Triticum aestivum) roots. PLoS One 10, e0138713
| Exogenous nitric oxide (NO) interferes with lead (Pb)-induced toxicity by detoxifying reactive oxygen species in hydroponically grown wheat (Triticum aestivum) roots.Crossref | GoogleScholarGoogle Scholar |
Konishi H, Kitano H, Komatsu S (2005) Identification of rice root proteins regulated by gibberellin using proteome analysis. Plant, Cell & Environment 28, 328–339.
| Identification of rice root proteins regulated by gibberellin using proteome analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXislKqs7g%3D&md5=6794571d1a55e41fc1ca60eef33a1b1cCAS |
Kopyra M, Gwozdz EA (2003) Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus. Plant Physiology and Biochemistry 41, 1011–1017.
| Nitric oxide stimulates seed germination and counteracts the inhibitory effect of heavy metals and salinity on root growth of Lupinus luteus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptlyluro%3D&md5=283fa377b8ea410c81f1db1505048d97CAS |
Kováčik J, Babula P, Klejdus B, Hedbavny J, Jarošová M (2014) Unexpected behavior of some nitric oxide modulators under cadmium excess in plant tissue. PLoS One 9, e91685
| Unexpected behavior of some nitric oxide modulators under cadmium excess in plant tissue.Crossref | GoogleScholarGoogle Scholar |
Kumar P, Tewari RK, Sharma PN (2010) Sodium nitroprusside-mediated alleviation of iron deficiency and modulation of antioxidant responses in maize plants. AoB Plants 2010, plq002
| Sodium nitroprusside-mediated alleviation of iron deficiency and modulation of antioxidant responses in maize plants.Crossref | GoogleScholarGoogle Scholar |
Liao WB, Huang GB, Yu JH, Zhang ML (2012) Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development. Plant Physiology and Biochemistry 58, 6–15.
| Nitric oxide and hydrogen peroxide alleviate drought stress in marigold explants and promote its adventitious root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1emsrnJ&md5=98bac4c9380f541c132722718ce7c63dCAS |
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranesCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXhs1Cgu78%3D&md5=39725a9fd4bc49e607b3b2823cadd6baCAS |
Lum HK, Lee CH, Butt YK, Lo SC (2005) Sodium nitroprusside affects the level of photosynthetic enzymes and glucose metabolism in Phaseolus aureus (mung bean). Nitric Oxide 12, 220–230.
| Sodium nitroprusside affects the level of photosynthetic enzymes and glucose metabolism in Phaseolus aureus (mung bean).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXks1ars7w%3D&md5=9b2eb2252f4d7a88d687daf1afcc4757CAS |
Manjunatha G, Gupta KJ, Lokesh V, Mur LA, Neelwarne B (2012) Nitric oxide counters ethylene effects on ripening fruits Plant Signaling & Behavior 7, 476–483.
| Nitric oxide counters ethylene effects on ripening fruitsCrossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xhs12ls7rM&md5=35a5448f05dfda5c6c526996c71bbc91CAS |
Meng Y, Liu F, Pang C, Fan S, Song M, Wang D, Li W, Yu S (2011) Label-free quantitative proteomics analysis of cotton leaf response to nitric oxide. Journal of Proteome Research 10, 5416–5432.
| Label-free quantitative proteomics analysis of cotton leaf response to nitric oxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOgu7bI&md5=ee7a2a61bcad3dba6829fc5cadc72352CAS |
Misra AN, Misra M, Singh R (2011) Nitric oxide ameliorates stress responses in plants. Plant, Soil and Environment 57, 95–100.
Mohannath G, Jackel JN, Lee YH, Buchmann RC, Wang H, Patil V, Adams AK, Bisaro DM (2014) A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis. PLoS One 9, e87592
| A complex containing SNF1-related kinase (SnRK1) and adenosine kinase in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Mur LAJ, Mandon J, Persijn S, Cristescu SM, Moshkov IE, Novikova GV, Hall MA, Harren FJ, Hebelstrup KH, Gupta KJ (2013) Nitric oxide in plants: an assessment of the current state of knowledge. AoB Plants 5, pls052
| Nitric oxide in plants: an assessment of the current state of knowledge.Crossref | GoogleScholarGoogle Scholar |
Negi S, Santisree P, Kharshiing EV, Sharma R (2010) Inhibition of the ubiquitin-proteasome pathway alters cellular levels of nitric oxide in tomato seedlings. Molecular Plant 3, 854–869.
| Inhibition of the ubiquitin-proteasome pathway alters cellular levels of nitric oxide in tomato seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1WhtbrO&md5=d3a925b9fa5afdffc16945071fe47ec3CAS |
Olsen AN, Ernst HA, Leggio LL, Skriver L (2005) KNAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10, 79–87.
| KNAC transcription factors: structurally distinct, functionally diverse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlajtrY%3D&md5=3ab29cadcd3582d69b8de62d2c7c6e29CAS |
Planchet E, Kaiser WM (2006) Nitric oxide production in plants: facts and fictions. Plant Signaling & Behavior 1, 46–51.
| Nitric oxide production in plants: facts and fictions.Crossref | GoogleScholarGoogle Scholar |
Procházková D, Haisel D, Wilhelmová N, Pavlíková D, Száková J (2013) Effects of exogenous nitric oxide on photosynthesis. Photosynthetica 51, 483–489.
| Effects of exogenous nitric oxide on photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Santisree P, Nongmaithem S, Vasuki H, Sreelakshmi Y, Ivanchenko MG, Sharma R (2011) Tomato root penetration in soil requires a coaction between ethylene and auxin signaling. Plant Physiology 156, 1424–1438.
| Tomato root penetration in soil requires a coaction between ethylene and auxin signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWksL4%3D&md5=9838ab80c9fb5d3dfb165fe83d900b0cCAS |
Santisree P, Bharnagar-Mathur P, Sharma KK (2015) NO to drought-multifunctional role of nitric oxide in plant drought. Do we have all the answers? Plant Science 239, 44–55.
| NO to drought-multifunctional role of nitric oxide in plant drought. Do we have all the answers?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVegtbnK&md5=db8259dd6ae14782e7264e3389c31adaCAS |
Schröder H (2006) No nitric oxide for HO-1 from sodium nitroprusside. Molecular Pharmacology 69, 1507–1509.
| No nitric oxide for HO-1 from sodium nitroprusside.Crossref | GoogleScholarGoogle Scholar |
Sehrawat A, Abat JK, Deswal R (2013) RuBisCO depletion improved proteome coverage of cold responsive S-nitrosylated targets in Brassica juncea. Frontiers in Plant Science 4, 342
Shen Z, Li P, Ni RJ, Ritchie M, Yang CP, Liu GF, Ma W, Liu GJ, Ma L, Li SJ, Wei ZG, Wang HX, Wang BC (2009) Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening. Molecular & Cellular Proteomics 8, 2443–2460.
| Label-free quantitative proteomics analysis of etiolated maize seedling leaves during greening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVSmsrfJ&md5=38b7203728412c9ddb88fb46b423faffCAS |
Sheokand S, Kumari A, Sawhney V (2008) Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants. Physiology and Molecular Biology of Plants 14, 355–362.
| Effect of nitric oxide and putrescine on antioxidative responses under NaCl stress in chickpea plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvVGmtrc%3D&md5=0c5da6551180b13220a8fb7f62e06acfCAS |
Shi HT, Ye T, Zhu JK, Chan Z (2014) Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis. Journal of Experimental Botany 65, 4119–4131.
| Constitutive production of nitric oxide leads to enhanced drought stress resistance and extensive transcriptional reprogramming in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGjsr%2FF&md5=60dbaabfa706180b05d7388edc1e4370CAS |
Shukla RK, Raha S, Tripathi V, Chattopadhyay D (2006) Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco. Plant Physiology 142, 113–123.
| Expression of CAP2, an APETALA2-family transcription factor from chickpea, enhances growth and tolerance to dehydration and salt stress in transgenic tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpvVKhsr8%3D&md5=62fbc676ec606e24bb12b8c70c92808eCAS |
Siddiqui MH, Al-Whaibi MH, Basalah MO (2011) Role of nitric oxide in tolerance of plants to abiotic stress. Protoplasma 248, 447–455.
| Role of nitric oxide in tolerance of plants to abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXovFCqur4%3D&md5=7482a6a84f61b0aa8a6485e86db24e08CAS |
Silveira NM, Oliveira JAD, Ribeiro C, Canatto RA, Siman L, Cambraia J, Farnese F (2015) Nitric oxide attenuates oxidative stress induced by arsenic in lettuce (Lactuca sativa) leaves. Water, Air, and Soil Pollution 226, 379
| Nitric oxide attenuates oxidative stress induced by arsenic in lettuce (Lactuca sativa) leaves.Crossref | GoogleScholarGoogle Scholar |
Tanou G, Job C, Rajjou L, Arc E, Belghazi M, Diamantidis G, Molassiotis A, Job D (2009) Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity. The Plant Journal 60, 795–804.
| Proteomics reveals the overlapping roles of hydrogen peroxide and nitric oxide in the acclimation of citrus plants to salinity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WhtrzF&md5=b5460d03011786d6279226438a2c9d5cCAS |
The UniProt Consortium (2015) UniProt: a hub for protein information. Nucleic Acids Research 43, D204–D212.
| UniProt: a hub for protein information.Crossref | GoogleScholarGoogle Scholar |
Tossi V, Amenta M, Lamattina L, Cassia R (2011) Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway. Plant, Cell & Environment 34, 909–921.
| Nitric oxide enhances plant ultraviolet-B protection up-regulating gene expression of the phenylpropanoid biosynthetic pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1SgtLs%3D&md5=aa264781a12d78e65ac8e47d1a746d94CAS |
Uchida A, Jagendorf AT, Hibino T, Takabe T (2002) Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice. Plant Science 163, 515–523.
| Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XntVejtLY%3D&md5=1dbed7b24a39a4aef496fa4810165a91CAS |
Wang Y, Suo B, Zhao T, Qu X, Yuan L, Zhao X, Zhao H (2011) Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering. Acta Physiologiae Plantarum 33, 1923–1932.
| Effect of nitric oxide treatment on antioxidant responses and psbA gene expression in two wheat cultivars during grain filling stage under drought stress and rewatering.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOntbrM&md5=93b79385ef43848924b548fb194dabeeCAS |
Wang Y, Luo Z, Du R, Liu Y, Ying T, Mao L (2013) Effect of nitric oxide on antioxidative response and proline metabolism in banana during cold storage. Journal of Agricultural and Food Chemistry 61, 8880–8887.
| Effect of nitric oxide on antioxidative response and proline metabolism in banana during cold storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1ymt7vJ&md5=2fdcff5724112b7254f901b7b513b564CAS |
Weinhold A, Wielsch N, Svatoš A, Baldwin IT (2015) Label-free nanoUPLC-MSE based quantification of antimicrobial peptides from the leaf apoplast of Nicotiana attenuata. BMC Plant Biology 15, 18
| Label-free nanoUPLC-MSE based quantification of antimicrobial peptides from the leaf apoplast of Nicotiana attenuata.Crossref | GoogleScholarGoogle Scholar |
Wienkoop S, Larrainzar E, Glinski M, González EM, Arrese-Igor C, Weckwerth W (2008) Absolute quantification of Medicago truncatula sucrose synthase isoforms and N-metabolism enzymes in symbiotic root nodules and the detection of novel nodule phosphoproteins by mass spectrometry. Journal of Experimental Botany 59, 3307–3315.
| Absolute quantification of Medicago truncatula sucrose synthase isoforms and N-metabolism enzymes in symbiotic root nodules and the detection of novel nodule phosphoproteins by mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWit7vK&md5=4588407743db39a10ccf8ac2c4a66b76CAS |
Yang L, Tian D, Todd CD, Luo Y, Hu X (2013) Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity. Journal of Proteome Research 12, 1316–1330.
| Comparative proteome analyses reveal that nitric oxide is an important signal molecule in the response of rice to aluminum toxicity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXoslOhsA%3D%3D&md5=1d6393d7f071df80a40f49a595f0c417CAS |
Yao YX, Dong QL, Zhai H, You CX, Hao YJ (2011) The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses. Plant Physiology and Biochemistry 49, 257–264.
| The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXit1ymt7g%3D&md5=c816d18d4f3bfd72f36e813b54a2498aCAS |
Yu M, Lamattina L, Spoel SH, Loake GJ (2014) Nitric oxide function in plant biology: a redox cue in deconvolution. New Phytologist 202, 1142–1156.
| Nitric oxide function in plant biology: a redox cue in deconvolution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnslyksL8%3D&md5=20ffab205642805c15792d614c592b59CAS |
Zhao X, Ding C, Chen L, Wang S, Wang Q, Ding Y (2012) Comparative proteomic analysis of the effects of nitric oxide on alleviating Cd-induced toxicity in rice (Oryza sativa L.) Plant Omics 5, 604–614.
Zheng Y, Hong H, Chen L, Li J, Sheng J, Shen L (2014) LeMAPK1, LeMAPK2, and LeMAPK3 are associated with nitric oxide-induced defense response against Botrytis cinerea in the Lycopersicon esculentum fruit. Journal of Agricultural and Food Chemistry 62, 1390–1396.
| LeMAPK1, LeMAPK2, and LeMAPK3 are associated with nitric oxide-induced defense response against Botrytis cinerea in the Lycopersicon esculentum fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXnsFahsw%3D%3D&md5=cd28ef59d377a13ddb4ba8c8e27bceabCAS |
