Differences between winter oilseed rape (Brassica napus L.) cultivars in nitrogen starvation-induced leaf senescence are governed by leaf-inherent rather than root-derived signals

. 2015 Jul ; 66 (13) : 3669-81. [epub] 20150504

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid25944925

Nitrogen (N) efficiency of winter oilseed rape (Brassica napus L.) line-cultivars (cvs.), defined as high grain yield under N limitation, has been primarily attributed to maintained N uptake during reproductive growth (N uptake efficiency) in combination with delayed senescence of the older leaves accompanied with maintained photosynthetic capacity (functional stay-green). However, it is not clear whether genotypic variation in N starvation-induced leaf senescence is due to leaf-inherent factors and/or governed by root-mediated signals. Therefore, the N-efficient and stay-green cvs. NPZ-1 and Apex were reciprocally grafted with the N-inefficient and early-senescing cvs. NPZ-2 and Capitol, respectively and grown in hydroponics. The senescence status of older leaves after 12 days of N starvation assessed by SPAD, photosynthesis and the expression of the senescence-specific cysteine protease gene SAG12-1 revealed that the stay-green phenotype of the cvs. NPZ-1 and Apex under N starvation was primarily under the control of leaf-inherent factors. The same four cultivars were submitted to N starvation for up to 12 days in a time-course experiment. The specific leaf contents of biologically active and inactive cytokinins (CKs) and the expression of genes involved in CK homeostasis revealed that under N starvation leaves of early-senescing cultivars were characterized by inactivation of biologically active CKs, whereas in stay-green cultivars synthesis, activation, binding of and response to biologically active CKs were favoured. These results suggest that the homeostasis of biologically active CKs was the predominant leaf-inherent factor for cultivar differences in N starvation-induced leaf senescence and thus N efficiency.

Zobrazit více v PubMed

Albacete Moreno A, Cantero AE, Grosskinsky D, et al. 2014. Ectopic overexpression of the cell wall invertase gene CIN1 increases water use efficiency in tomato (

Arvidsson S, Kwasniewski M, Diego M, Riaño-Pachón DM, Mueller-Roeber B. 2008. QuantPrime—a flexible tool for reliable high-throughput primer design for quantitative PCR. BMC Bioinformatics doi: 10.1186/1471-2105-9-465. PubMed PMC

Balazadeh S, Riaño-Pachón DM, Mueller-Roeber B. 2008. Transcription factors regulating leaf senescence in PubMed

Balibrea Lara ME, Gonzalez MCG, Fatima T, Ehneß T, Lee TK, Roels R, Tanner W, Roitsch T. 2004. Extracellular invertase is an essential component of cytokinin mediated delay of senescence. Plant Cell 16, 1276–1287. PubMed PMC

Berry PM, Spink J, Foulkes MJ, White PJ. 2010. The physiological basis of genotypic differences in nitrogen use efficiency in oilseed rape (

Buchanan-Wollaston V. 1997. The molecular biology of leaf senescence. Journal of Experimental Botany 48, 181–199.

Dai J, Dong H. 2011. Stem girdling influences concentration of endogenous cytokinins and abscisic acid in relation to leaf senescence in cotton. Acta Physiologiae Plantarum 33, 1697–1705.

del Mar Rubio-Wilhelmi M, Reguera M, Sanchez-Rodriguez E, Romero L, Blumwald E, Ruiz JM. 2014. P

Desclos M, Dubousset L, Etienne P, Le Caherec F, Satoh H, Bonnefoy J, Ourry A, Avice JC. 2008. A proteomic approach to reveal a novel role of PubMed PMC

Dong H, Niu Y, Li W, Zhang D. 2008. Effects of cotton rootstock on endogenous cytokinins and abscisic acid in xylem sap and leaves in relation to leaf senescence. Journal of Experimental Botany 59, 1295–1304. PubMed

Etienne P, Desclos M, Gou LL, Gombert J, Bonnefoy J, Maurel K, Le Dily F, Ourry A, Avice JC. 2007. N-protein mobilisation associated with the leaf senescence process in oilseed rape is concomitant with the disappearance of trypsin inhibitor activity. Functional Plant Biology 34, 895–906. PubMed

Evans JR. 1989. Photosynthesis and nitrogen relationships in leaves of C3 plants. Oecologia 78, 9–19. PubMed

Gajdošová S, Spíchal L, Kamínek M. 2011. Distribution, biological activities, metabolism, and the conceivable function of PubMed

Galuszka P, Popelková H, Werner T, Frébortová J, Pospísilová H, Mik V, Köllmer I, Schmülling T, Frébort I. 2007. Biochemical characterization of cytokinins oxidases/dehydrogenases from

Gan S, Amasino RM. 1995. Inhibition of leaf senescence by autoregulated production of cytokinins. Science 270, 1986–1988. PubMed

Grbić V. 2003. SAG2 and SAG12 protein expression in senescing Arabidopsis plants. Physiologia Plantarum 119, 263–269.

Gregersen PL, Culetic A, Boschian L, Krupinska K. 2013. Plant senescence and crop productivity. Plant Molecular Biology 82, 603–622. PubMed

Großkinsky DK, Albacete A, Jammer A, Krbez P, van der Graaff E, Pfeifhofer H, Roitsch T. 2014. A rapid phytohormone and phytoalexin screening method for physiological phenotyping. Molecular Plant 7, 1053–1056. PubMed

He P, Osaki M, Takebe M, Shinano T, Wasaki J. 2005. Endogenous hormones and expression of senescence-related genes in different senescent types of maize. Journal of Experimental Botany 56, 1117–1128 PubMed

Hou B, Lim EK, Higgins GS, Bowles DJ. 2004. N-glucosylation of cytokinins by glycosyltransferases of PubMed

Jin SH, Ma XM, Kojima M, Sakakibara H, Wang YW, Hou BK. 2013. Overexpression of glucosyltransferase PubMed

Kamh M, Wiesler F, Ulas A, Horst WJ. 2005. Root growth and N-uptake of oilseed rape (Brassica napus L.) cultivars differing in nitrogen efficiency. Journal of Plant Nutrition and Soil Science 168, 130–137.

Kim HJ, Hojin R, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, Nam HG, Hwang I. 2006. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in PubMed PMC

Koeslin-Findeklee F, Meyer A, Girke A, Beckmann K, Horst WJ. 2014. The superior nitrogen efficiency of winter oilseed rape (

Koeslin-Findeklee F, Safavi Rizi V, Becker MA, Parra-Londono S, Arif M, Balazadeh S, Mueller-Roeber M, Kunze R, Horst WJ. 2015. Transcriptomic analysis of nitrogen starvation- and cultivar-specific leaf senescence in winter oilseed rape ( PubMed

Kowalska M, Galuszka P, Frébortová J, Ŝebela M, Béres T, Hluska T, Ŝmehilová M, Bilyeu KD, Frébort I. 2010. Vacuolar and cytosolic cytokinin dehydrogenases of PubMed

Köllmer I, Novák O, Strnad M, Schmülling T, Werner T. 2014. Overexpression of the cytosolic cytokinin oxidase/dehydrogenase ( PubMed

Kuroha T, Tokungaga H, Kojima M, Ueda N, Ishida T, Nagawa S, Fukuda H, Sugimoto K, Sakakibara H. 2009. Functional analyses of PubMed PMC

Kusaba M, Tanaka A, Tanaka R. 2013. Stay-green plants: what do they tell us about the molecular mechanism of leaf senescence. Photosynthesis Research 117, 221–234. PubMed

Lim PO, Kim HJ, Nam HG. 2007. Leaf senescence. Annual Review of Plant Biology 58, 115–136. PubMed

Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2 PubMed

Miyawaki K, Matsumoto-Kitano M, Kakimoto T. 2004. Expression of cytokinin biosynthetic isopentenyltransferaes genes in PubMed

Moroni JS. 1997. Studies on the efficiency of rapeseed (

Parlitz S, Kunze R, Mueller-Roeber B, Balazadeh S. 2011. Regulation of photosynthesis and transcription factor expression by leaf shading and re-illumination in PubMed

Rauf M, Arif M, Dortay H, Matallana-Ramírez LP, Waters MT, Nam HG, Lim PO, Mueller-Roeber B, Balazadeh S. 2013. PubMed PMC

Sakakibara H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57, 431–449. PubMed

Sakuraba Y, Balazadeh S, Tanaka R, Mueller-Roeber B, Tanaka A. 2012a. Overproduction of chl B retards senescence through transcriptional reprogramming in PubMed

Sakuraba Y, Schelbert S, Park SY, Han SH, Lee BD, Andrès CB, Kessler F, Hörtensteiner S, Paeck NC. 2012b. Stay-green and chlorophyll catabolic enzymes interact at light-harvesting complex II for chlorophyll detoxification during leaf senescence in PubMed PMC

Schmitz RY, Skoog F, Playtis AJ, Leonard NJ. 1972. Cytokinins: synthesis and biological activity of geometric and position isomers of zeatin. Plant Physiology 50, 702–705. PubMed PMC

Schmülling T, Werner T, Riefler M, Krupková E, Bartina y Manns B. 2003. Structure and function of cytokinin oxidase/dehydrogenase genes of maize, rice, PubMed

Schmülling T. 2004. Cytokinin. In: Lennarz W and Lane MD, eds. Encyclopedia of Biological Chemistry. Academic Press/Elsevier Science.

Schulte auf’m Erley G, Wijaya KA, Ulas A, Becker H, Wiesler F, Horst WJ. 2007. Leaf senescence and N uptake parameters as selection traits for nitrogen efficiency of oilseed rape cultivars. Physiologia Plantarum 130, 519–531.

Schulte auf’m Erley G, Ambebe TF, Worku M, Bänzinger M, Horst WJ. 2010. Photosynthesis and leaf-nitrogen dynamics during leaf senescence of tropical maize cultivars in hydroponics in relation to N efficiency in the field. Plant and Soil 330, 313–328.

Schulte auf’m Erley G, Behrens T, Ulas A, Wiesler F, Horst WJ. 2011. Agronomic traits contributing to nitrogen efficiency of winter oilseed rape cultivars. Field Crops Research 124, 114–123.

Smart CM. 1994. Gene expression during leaf senescence. New Phytologist 126, 419–448. PubMed

Steibel JP, Poletto R, Coussens PM, Rosa GJM. 2009. A powerful and flexible linear mixed model framework for the analysis of relative quantification RT-PCR data. Genomics 94, 146–152. PubMed

Thomas H, Howarth CJ. 2000. Five ways to stay green. Journal of Experimental Botany 51, 329–337. PubMed

Thomas H, Ougham H. 2014. The stay-green trait. Journal of Experimental Botany 65, 3889–3900. PubMed

Tokunaga H, Kojima M, Kuroha T, Ishida T, Sugimoto K, Kiba T, Sakakibara H. 2012. PubMed

Trifunović M, Cingel A, Simonović A, Jevremović S, Petrić M, Dragićević IC, Motyka V, Bobrev PI, Zahajská L, Subotić A. 2013. Overexpression of Arabidopsis cytokinin oxidase/dehydrogenase genes

Wang A, Li Y, Zhang C. 2012. QTL mapping for stay-green in maize (

Wang J, Ma XM, Kojima M, Sakakibara H, Hou BK. 2013. Glucosyltransgerase PubMed

Wingler A, Roitsch T. 2008. Metabolic regulation of leaf senescence: interactions of sugar signalling with biotic and abiotic stress responses. Plant Biology 10, 50–62. PubMed

Zwack PJ, Rashotte AM. 2013. Cytokinin inhibition on leaf senescence. Plant Signal and Behavior 8, e24737; http://dx.doi.org/10.4161/psb.24737 PubMed PMC

Najít záznam

Citační ukazatele

Pouze přihlášení uživatelé

Možnosti archivace

Nahrávání dat ...