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Grain yield and nitrogen use efficiency are increased by exogenous cytokinin application through the improvement in root physiological traits of rice

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Abstract

Cytokinins play crucial roles in plant growth and development. However, the mechanism underlying their regulation to the grain yield and nitrogen use efficiency (NUE) in rice (Oryza sativa L.) remains unclear. The purpose of this study was to elucidate the issue. Two types of rice varieties, the N-efficient variety and N-inefficient variety, were grown in a paddy field under 180 kg N hm− 2 with three chemicals applied to leaves at heading time including control (spraying distilled water), spraying 6-benzylaminopurine (6-BA), and spraying an inhibitor of cytokinins synthesis, lovastatin (Lov). Results showed that the 6-BA treatment significantly increased grain yield and internal NUE in both varieties when compared with the control, and the results were reversed under the Lov treatment. The N-efficient variety showed better potential and stability than the N-inefficient variety in yield performance under 6-BA and Lov treatments. The improved grain yield and internal NUE by applying 6-BA were mainly due to the increased filled grain percentage, greater canopy photosynthetic rate (CPR) and more N allocated from stems and leaves to panicles (i.e., greater panicle N accumulation at maturity, PNAM). Both CPR and PNAM were closely associated with root oxidation activity, root soluble sugars and cytokinin contents, activities of antioxidant enzymes and the expression level of genes related to nitrogen transport in roots during grain filling. The results suggested that cytokinins could synergistically increase grain yield and NUE of rice by enhancing photosynthetic production and nitrogen partitioning efficiency as a result of improved root physiological traits during grain filling.

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References

  • Ali S, Bai P, Zeng F, Cai S, Shamsi IH, Qiu B, Wu FB, Zhang GP (2011) The ecotoxicological and interactive effects of chromium and aluminum on growth, oxidative damage and antioxidant enzymes on two barley genotypes differing in Al tolerance. Environ Exp Bot 70(2–3):185–191

    Article  CAS  Google Scholar 

  • Boonman A, Prinsen E, Gilmer F, Schurr U, Peeters AJ, Voesenek LA, Pons TL (2007) Cytokinin import rate as a signal for photosynthetic acclimation to canopy light gradients. Plant Physiol 143:1841–1852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chu G, Chen T, Chen S, Xu C, Wang D, Zhang X (2018) Agronomic performance of drought-resistance rice cultivars grown under alternate wetting and drying irrigation management in southeast China. Crop J 6:482–494

    Article  Google Scholar 

  • Chu G, Chen S, Xu C, Wang D, Zhang X (2019) Agronomic and physiological performance of indica/japonica hybrid rice cultivar under low nitrogen conditions. Field Crop Res 243:107625

    Article  Google Scholar 

  • Dhugga KS, Waines JG (1989) Analysis of nitrogen accumulation and use in bread and durum wheat. Crop Sci 29:1232–1239

    Article  Google Scholar 

  • Dong MH, Chen PF, Xie YL, Qiao ZY, Yang JC (2012) Variations in carbohydrate and protein accumulation among spikelets at different positions within a panicle during rice grain filling. Rice Sci 19(3):223–232

    Article  Google Scholar 

  • Fageria NK (2014) Nitrogen harvest index and its association with crop yields. J plant nutr 37(6):795–810

    Article  CAS  Google Scholar 

  • Fang XM, Li YS, Nie J, Wang C, Huang KH, Zhang YK, Zhang YL, She HZ, Liu XB, Ruan RW, Yuan XH, Yi ZL (2018) Effects of nitrogen fertilizer and planting density on the leaf photosynthetic characteristics, agronomic traits and grain yield in common buckwheat (Fagopyrum esculentum M.). Field Crops Res 219:160–168

    Article  Google Scholar 

  • Fowler DB (2003) Crop nitrogen demand and grain protein concentration of spring and winter wheat. Agr J 95:260–265

    Article  Google Scholar 

  • Gregersen PL, Culetic A, Boshian L, Krupinska K (2013) Plant senescence and crop productivity. Plant Mol Biol 82:603–622

    Article  CAS  PubMed  Google Scholar 

  • Gu JF, Chen Y, Zhang H, Li ZK, Zhou Q, Yu C, Kong XS, Liu LJ, Wang ZQ, Yang JC (2017) Canopy light and nitrogen distributions are related to grain yield and nitrogen use efficiency in rice. Field Crop Res 206:74–85

    Article  Google Scholar 

  • Gu JF, Li ZK, Mao YQ, Struik PC, Zhang H, Liu LJ, Wang ZQ, Yang JC (2018) Roles of nitrogen and cytokinin signals in root and shoot communications in maximizing of plant productivity and their agronomic applications. Plant Sci 274:320–331

    Article  CAS  PubMed  Google Scholar 

  • Ioio RD, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S (2008) A genetic framework for the control of cell division and differentiation in the root meristem. Science 322(5906):1380–1384

    Article  Google Scholar 

  • Jameson PE, Song JC (2016) Cytokinin: a key driver of seed yield. J Exp Bot 67:593–606

    Article  PubMed  Google Scholar 

  • Ju CX (2017) Agronomic and physiological traits for rice cultivars differing in response to nitrogen. Ph D thesis, Yangzhou Univsity, Yangzhou, Jiangsu, China. (in Chinese)

  • Ju CX, Buresh RJ, Wang ZQ, Zhang H, Liu LJ, Yang JC, Zhang JH (2015) Root and shoot traits for rice varieties with higher grain yield and higher nitrogen use efficiency at lower nitrogen rates application. Field Crops Res 175:47–55

    Article  Google Scholar 

  • Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. J Exp Bot 62(4):1399–1409

    Article  CAS  PubMed  Google Scholar 

  • Kiba T, Yamada H, Sato S, Kato T, Tabata S, Yamashino T, Mizuno T (2003) The type-A response regulator, ARR15, acts as a negative regulator in the cytokinin-mediated signal transduction in Arabidopsis thaliana. Plant and Cell Physiol 44(8):868–874

    Article  CAS  Google Scholar 

  • Krouk G, Ruffel S, Gutierrez RA, Gojon A, Crawford NM, Coruzzi GM, Lacombe B (2011) A framework integrating plant growth with hormones and nutrients. Trends Plant Sci 16 (2011): 178–182

  • Li S, Song M, Duan J, Yang J, Zhu Y, Zhou S (2019) Regulation of Spraying 6-BA in the Late Jointing Stage on the Fertile Floret Development and Grain Setting in Winter Wheat. Agronomy 9(9):546

    Article  CAS  Google Scholar 

  • Liu K, Li TT, Chen Y, Huang J, Qiu YY, Li SY, Wang H, Zhu A, Zhuo XX, Yu F, Zhang H, Gu JF, Liu LJ, Yang JC (2020) Effects of root morphology and physiology on the formation and regulation of large panicles in rice. Field Crops Res 258:107946

    Article  Google Scholar 

  • Lu MZ, Snyder R, Grant J, Tegeder M (2020) Manipulation of sucrose phloem and embryo loading affects pea leaf metabolism, carbon and nitrogen partitioning to sinks as well as seed storage pools. The Plant J 101(1):217–236

    Article  CAS  PubMed  Google Scholar 

  • Marhavý P, Duclercq J, Weller B, Feraru E, Bielach A, Offringa R, Friml J, Schwechheimer C, Murphy A, Benková E (2014) Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr Biol 24(9):1031–1037

    Article  PubMed  Google Scholar 

  • Mclntyre KE, Bush DR, Argueso CT (2021) Cytokinin regulation of source-sink relationships in plant-pathogen interactions. Front Plant Sci 12:585

    Google Scholar 

  • Nishimura C, Ohashi Y, Sato S, Kato T, Tabata S, Ueguchi C (2004) Genetic analysis of Arabidopsis histidine kinase genes encoding cytokinin receptors reveals their overlapping biological functions in the regulation of shoot and root growth in Arabidopsis thaliana. Plant Cell 16:1365–1377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu S, Wu M, Han YI, Xia J, Zhang ZHE, Yang H, Wan S (2010) Nitrogen effects on net ecosystem carbon exchange in a temperate steppe. Global Change Biol 16(1):144–155

    Article  Google Scholar 

  • Ntanos DA, Koutroubas SD (2002) Dry matter and N accumulation and translocation for Indica and Japonica rice under Mediterranean conditions. Field Crops Res 74(1):93–101

    Article  Google Scholar 

  • Osaki M, Shinano T, Matsumoto M, Zheng T, Tadano T (1997) A root-shoot interaction hypothesis for high productivity of fifield crops. Soil Sci Plant Nutr 37:445–454

    Article  Google Scholar 

  • Osugi A, Sakakibara H (2015) Q&A: How do plants respond to cytokinins and what is their importance? BMC bio, 13(1):1–10

    Article  Google Scholar 

  • Pan S, Rasul F, Li W, Tian H, Mo Z, Duan M, Tang X (2013) Roles of plant growth regulators on yield, grain qualities and antioxidant enzyme activities in super hybrid (Oryza sativa L.). Rice 6(1):1–10

    Article  Google Scholar 

  • Pan X, Welti R, Wang X (2010) Quantitative analysis of major plant hormones incrude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat Protoc 5:986–992

    Article  CAS  PubMed  Google Scholar 

  • Peleg Z, Reguera M, Tumimbang E, Walia H, Blumwald E (2011) Cytokinin mediated source/sink modifications improve drought tolerance and increase grain yield in rice under water stress. Plant Biotechnol J 9(7):747–758

    Article  CAS  PubMed  Google Scholar 

  • Ramasamy S, Berge HFM, Purushothaman S (1997) Yield formation in rice in response to drainage and nitrogen application. Field Crops Res 51:65–82

    Article  Google Scholar 

  • Rawyler A, Arpagaus S, Braendle R (2002) Impact of oxygen stress and energy availability on membrane stability of plant cells. Ann Bot 90(4):499–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rieflfler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18:40–54

    Article  Google Scholar 

  • Ren B, Zhu Y, Zhang J, Dong S, Liu P, Zhao B (2016) Effects of spraying exogenous hormone 6-benzyladenine (6-BA) after waterlogging on grain yield and growth of summer maize. Field Crops Res 188:96–104

    Article  Google Scholar 

  • Sakakibara H, Takei K, Hirose N (2006) Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci 11(9):440–448

    Article  CAS  PubMed  Google Scholar 

  • Shao G, Chen M, Wang W, Mou R, Zhang G (2007) Iron nutrition affects cadmium accumulation and toxicity in rice plants. Plant Growth Regul 53(1):33–42

    Article  CAS  Google Scholar 

  • Sun DC, Li YL, Zhao XY, Zuo XA, Mao W (2015) Effects of enclosure and grazing on carbon and water fluxes of sandy grassland. Chin J Plant Ecol 6:565–576

    Google Scholar 

  • Takei K, Sakakibara H, Taniguchi, Sugiyama T (2001) Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: Implication ofcytokinin species that induces gene expression of maize response regulator. Plant Cell Physiol 42(1):85–93

    Article  CAS  PubMed  Google Scholar 

  • Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant Cell Physiol 45:1053–1062

    Article  CAS  PubMed  Google Scholar 

  • Veltman RH, Lenthéric I, van der Plas LHW, Peppelenbos HW (2003) Internal browning in pear fruit (Pyrus communis L. cv. Conference) may be a result of a limited availability of energy and antioxidants. Postharvest Bio Tec 28 (2): 295–302

  • Wang H, Zhang Y, Chen A, Liu H, Zhai L, Lei B, Ren T (2017) An optimal regional nitrogen application threshold for wheat in the North China Plain considering yield and environmental effects. Field Crops Res 207:52–61

    Article  Google Scholar 

  • Wang JL, Fu ZS, Chen GF, Zou GY, Song XF, Liu FX (2018) Runoff nitrogen (N) losses and related metabolism enzyme activities in paddy field under different nitrogen fertilizer levels. Environ Sci Pollut R 25:27583–27593

    Article  CAS  Google Scholar 

  • Wang XT, Suo YY, Feng Y, Shohag MJI, Gao J, Zhang QC, Xie S, Lin XY (2011) Recovery of N15 labeled urea and soil nitrogen dynamics as affected by irrigation management and nitrogen application rate in a double rice cropping system. Plant Soil 343:195–208

    Article  CAS  Google Scholar 

  • Wang ZQ, Zhang WY, Beebout SS, Zhang H, Liu LJ, Yang JC, Zhang JH (2016) Grain yield, water and nitrogen use efficiencies of rice as influenced by irrigation regimes and their interaction with nitrogen rates. Field Crops Res 193:54–69

    Article  Google Scholar 

  • Werner T, Köllmer I, Bartrina I, Holst K, Schmülling T (2006) New insights into the biology of cytokinin degradation. Plant bio 8(03):371–381

    Article  CAS  Google Scholar 

  • Werner T, Nehnevajova E, Köllmer I, Novák O, Strnad M, Krämer U, Schmülling T (2010) Root-specifific reduction of cytokinin causes enhanced root growth, drought tolerance, and leaf mineral enrichment in arabidopsis and tobacco. Plant Cell 22:3905–3920

    Article  PubMed  PubMed Central  Google Scholar 

  • Wu H, Xiang J, Zhang Y, Zhang Y, Peng S, Chen H, Zhu D (2018) Effects of post-anthesis nitrogen uptake and translocation on photosynthetic production and rice yield. Sci Rep 8:12891

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu CM, Wang DY, Chen S, Chen LP, Zhang XF (2013) Effects of aeration on root physiology and nitrogen metabolism in rice. Rice Sci 20(2):148–153

    Article  Google Scholar 

  • Xu GW, Zhang JH, Lam HM, Wang ZQ, Yang JC (2007) Hormonal changes are related to the poor grain filling in the inferior spikelets of rice cultivated under non-flooded and mulched condition. Field Crops Res 101(1):53–61

    Article  Google Scholar 

  • Xue YG, Duan H, Liu LJ, Wang ZQ, Yang JC, Zhang JH (2013) An improved crop management increases grain yield and nitrogen and water use efficiency in rice. Crop Sci 53:271–284

    Article  Google Scholar 

  • Xu YJ, Li K, Zhu KY, Tian Y, Yu Q, Zhang WY, Wang ZQ (2020) Effect of exogenous plant hormones on agronomic and physiological performance of a leaf early-senescent rice mutant osled. Plant Growth Regul 92(3):517–533

    Article  CAS  Google Scholar 

  • Yang JC, Zhang JH (2010) Grain-fifilling problem in ‘super’ rice. J Exp Bot 61:1–5

    Article  CAS  PubMed  Google Scholar 

  • Yang JC, Zhang JH, Wang ZQ, Zhu QS, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant physiol 127(1):315–323

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice. International Rice Research Institute, The Philippines, pp 24–79

    Google Scholar 

  • Zaka R, Vandecasteele CM, Misset MT (2002) Effects of low chronic doses of ionizing radiation on antioxidant enzymes and G6PDH activities in Stipa capillata (Poaceae). J Exp Bot 53(376):1979–1987

    Article  CAS  PubMed  Google Scholar 

  • Zhang H, Liu K, Wang ZQ, Liu LJ, Yang JC (2015a) Abscisic acid, ethylene and antioxidative systems in rice grains in relation with grain filling subjected to postanthesis soil-drying. Plant Growth Regul 76(2):135–146

    Article  CAS  Google Scholar 

  • Zhang H, Xue YG, Wang ZQ, Yang JC, Zhang JH (2009a) Morphological and physiological traits of roots and their relationships with shoot growth in “super” rice. Field Crops Res 113(1):0–40

    Article  Google Scholar 

  • Zhang H, Tan GL, Yang LN, Yang JC, Zhang JH, Zhao BH (2009b) Hormones in the grains and roots in relation to post-anthesis development of inferior and superior spikelets in japonica/indica hybrid rice. Plant Physiol Bioch 47(3):195–204

    Article  CAS  Google Scholar 

  • Zhang YK, Zhu DF, Zhang YP, Chen HZ, Xiang J, Lin XQ (2015b) Low pH-induced changes of antioxidant enzyme and ATPase activities in the roots of rice (Oryza sativa L.) seedlings. PLoS ONE 10(2):e0116971

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang WY, Cao ZQ, Zhou Q, Chen J, Xu GW, Gu JF, Liu LJ, Wang ZQ, Yang JC, Zhang H (2016) Grain filling characteristics and their relations with endogenous hormones in large-and small-grain mutants of rice. PLoS ONE 11(10):e0165321

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu KY, Yan JQ, Shen Y, Zhang WY, Xu YJ, Wang ZQ, Yang JC (2021) Deciphering the physio-morphological traits for high yield potential in nitrogen efficient varieties (NEVs): A japonica rice case study. J Integr Agr 20(0):2–19

    CAS  Google Scholar 

  • Zhu KY, Zhou Q, Shen Y, Yan JQ, Xu YJ, Wang ZQ, Yang JC (2020) Agronomic and physiological performance of an indica-japonica rice variety with a high yield and high nitrogen use efficiency. Crop Sci 60(3):1556–1568

    Article  CAS  Google Scholar 

  • Zhou AJ (2002) Relationships of changes in cytokinin concentrations in the roots and grains during grain filling of rice with the filling of grains and their regulation. Master thesis, Yangzhou University, Yangzhou, Jiangsu, China. (in Chinese)

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Funding

The research was supported by the National Natural Science Foundation of China (32071943, 31901444, 31901445), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD-1), the Top Talent Supporting Program of Yangzhou University (2015-01), the Provincial Natural Science Foundation of Jiangsu (BK20190880), and the Natural Science Foundation of the Jiangsu Higher Education Institutions (19KJB210019).

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  1. Jiangsu Key Lab. of Crop Genetics and Physiology, Jiangsu Key Laboratory of Crop Cultivation and Physiology, Agricultural College of Yangzhou University, 225009, Yangzhou, China

    Kuanyu Zhu, Weichen Ren, Jiaqian Yan, Yajun Zhang, Weiyang Zhang, Zhiqin Wang & Jianchang Yang

  2. Jiangsu Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, 225009, Yangzhou, China

    Kuanyu Zhu, Weichen Ren, Jiaqian Yan, Yajun Zhang, Weiyang Zhang, Zhiqin Wang & Jianchang Yang

  3. Joint International Research Laboratory of Agriculture and Agri-product Safety, the Ministry of Education of China, Yangzhou University, 225009, Yangzhou, Jiangsu, China

    Yunji Xu

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  1. Kuanyu Zhu
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Zhu, K., Ren, W., Yan, J. et al. Grain yield and nitrogen use efficiency are increased by exogenous cytokinin application through the improvement in root physiological traits of rice. Plant Growth Regul 97, 157–169 (2022). https://doi.org/10.1007/s10725-022-00808-x

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