Effect of soluble sugar content in silique wall on seed oil accumulation during the seed-filling stage in Brassica napus
Fei Ni A , Jiahuan Liu A , Jing Zhang A , Mohammad Nauman Khan A , Tao Luo A , Zhenghua Xu
A B and Liyong Hu A B
+ Author Affiliations
- Author Affiliations
A MOA Key Laboratory of Crop Ecophysiology and Farming System in the Middle Reaches of the Yangtze River/College of Plant Science and Technology, Huazhong Agricultural University, Wuhan 430070, Hubei, China.
B Corresponding authors. Email: liyonghu@mail.hzau.edu.cn; xzh@mail.hzau.edu.cn
Crop and Pasture Science 69(12) 1251-1263 https://doi.org/10.1071/CP17392
Submitted: 20 October 2017 Accepted: 1 October 2018 Published: 6 December 2018
Abstract
Soluble sugar content in silique wall and seeds of rapeseed (Brassica napus L.) has significant effects on seed oil formation and accumulation. We studied the relationship between soluble sugar content in B. napus seeds and silique wall and oil concentration under field conditions in two cropping seasons, and examined changes in soluble sugar content in seeds and silique wall under different nitrogen (N) levels. Two commercialised Chinese rapeseed varieties, HZ9 and HZ62, with high seed yield and different N responses were used. Our results indicated that carbon (C) : N ratio and soluble sugar content in silique wall had the greater effect on seed oil concentration. When C : N ratio and soluble sugar content in silique wall were within 5–15% and 10–25%, respectively, plants had relatively well coordinated C and N metabolism, facilitating oil accumulation. During 25–35 days of silique development, when C : N ratio and soluble sugar content in silique wall were within 10–15 and 15–25%, respectively, oil synthesis was fastest; the highest accumulation rate was 3.8% per day. When they were each <5%, seeds tended to mature, and oil synthesis gradually decreased, ceased or degraded. During the early stage of silique development, if C : N ratio and soluble sugar content in silique wall were >15% and 30%, there was no apparent tendency for oil accumulation, probably because of adverse environmental conditions. When N application increased from 0 to 270 kg ha–1, final oil concentration in seeds decreased by 0.024%. In summary, C : N ratio and soluble sugar content in silique wall are important in regulating seed oil concentration, whereas excessive N application significantly reduced seed oil concentration. Therefore, appropriate reduction of N application would save resources, provide environment benefits and increase rapeseed oil production with no substantial reduction in seed yield, through coordinated seed yield and oil concentration.
Additional keywords: canola, chlorophyll, nitrogen fertiliser.
References
Bennett EJ, Roberts JA, Wagstaff C (2011) The role of the silique in seed development: strategies for manipulating yield. New Phytologist 190, 838–853.| The role of the silique in seed development: strategies for manipulating yield.Crossref | GoogleScholarGoogle Scholar |
Brennan RF, Bolland MDA (2009) Comparing the nitrogen and phosphorus requirements of canola and wheat for grain yield and quality. Crop & Pasture Science 60, 566–577.
| Comparing the nitrogen and phosphorus requirements of canola and wheat for grain yield and quality.Crossref | GoogleScholarGoogle Scholar |
Diepenbrock W (2000) Yield analysis of winter oilseed rape (Brassica napus L.): A review. Field Crops Research 67, 35–49.
| Yield analysis of winter oilseed rape (Brassica napus L.): A review.Crossref | GoogleScholarGoogle Scholar |
Diepenbrock W, Geisler G (1979) Compositional changes in developing pods and seeds of oilseed rape (Brassica napus L.) as affected by pod position on the plant. Canadian Journal of Plant Science 59, 819–830.
| Compositional changes in developing pods and seeds of oilseed rape (Brassica napus L.) as affected by pod position on the plant.Crossref | GoogleScholarGoogle Scholar |
Dubousset L, Etienne P, Avice JC (2010) Is the remobilization of S and N reserves for seed filling of winter oilseed rape modulated by sulphate restrictions occurring at different growth stages? Journal of Experimental Botany 61, 4313–4324.
| Is the remobilization of S and N reserves for seed filling of winter oilseed rape modulated by sulphate restrictions occurring at different growth stages?Crossref | GoogleScholarGoogle Scholar |
Eastmond P, Koláčná L, Rawsthorne S (1996) Photosynthesis by developing embryos of oilseed rape (Brassica napus L.). Journal of Experimental Botany 47, 1763–1769.
| Photosynthesis by developing embryos of oilseed rape (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |
Franzaring J, Gensheimer G, Weller S, Schmid I, Fangmeier A (2012) Allocation and remobilisation of nitrogen in spring oilseed rape (Brassica napus L. cv. Mozart) as affected by N supply and elevated CO2. Environmental and Experimental Botany 83, 12–22.
| Allocation and remobilisation of nitrogen in spring oilseed rape (Brassica napus L. cv. Mozart) as affected by N supply and elevated CO2.Crossref | GoogleScholarGoogle Scholar |
Fritschi FB, Ray JD (2007) Soybean leaf nitrogen, chlorophyll content, and chlorophyll a/b ratio. Photosynthetica 45, 92–98.
| Soybean leaf nitrogen, chlorophyll content, and chlorophyll a/b ratio.Crossref | GoogleScholarGoogle Scholar |
Fu S, Li C, Ni M, Tang L, Qi C (2014) Meteorological factors on the influence of the rape seed oil accumulation. Chinese Bulletin of Botany 49, 41–48.
| Meteorological factors on the influence of the rape seed oil accumulation.Crossref | GoogleScholarGoogle Scholar |
García-Inza GP, Castro DN, Hall AJ, Rousseaux MC (2014) Responses to temperature of fruit dry weight, oil concentration, and oil fatty acid composition in olive (Olea europaea L. var. ‘Arauco’). European Journal of Agronomy 54, 107–115.
| Responses to temperature of fruit dry weight, oil concentration, and oil fatty acid composition in olive (Olea europaea L. var. ‘Arauco’).Crossref | GoogleScholarGoogle Scholar |
Gitelson AA, Gritz Y, Merzlyak MN (2003) Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves. Journal of Plant Physiology 160, 271–282.
| Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves.Crossref | GoogleScholarGoogle Scholar |
Hamzei J (2011) Seed, oil, and protein yields of canola under combinations of irrigation and nitrogen application. Agronomy Journal 103, 1152
| Seed, oil, and protein yields of canola under combinations of irrigation and nitrogen application.Crossref | GoogleScholarGoogle Scholar |
Harwood JL, Guschina IA (2013) Regulation of lipid synthesis in oil crops. FEBS Letters 587, 2079–2081.
| Regulation of lipid synthesis in oil crops.Crossref | GoogleScholarGoogle Scholar |
Hua W, Li RJ, Zhan GM, Liu J, Li J, Wang XF, Liu GH, Wang HZ (2012) Maternal control of seed oil content in Brassica napus: the role of silique wall photosynthesis. The Plant Journal 69, 432–444.
| Maternal control of seed oil content in Brassica napus: the role of silique wall photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Hua S, Chen Z-H, Zhang Y, Yu H, Lin B, Zhang D (2014) Chlorophyll and carbohydrate metabolism in developing silique and seed are prerequisite to seed oil content of Brassica napus L. Botanical Studies 55, 34
| Chlorophyll and carbohydrate metabolism in developing silique and seed are prerequisite to seed oil content of Brassica napus L.Crossref | GoogleScholarGoogle Scholar |
Huarancca Reyes T, Scartazza A, Lu Y, Yamaguchi J, Guglielminetti L (2016) Effect of carbon/nitrogen ratio on carbohydrate metabolism and light energy dissipation mechanisms in Arabidopsis thaliana. Plant Physiology and Biochemistry 105, 195–202.
| Effect of carbon/nitrogen ratio on carbohydrate metabolism and light energy dissipation mechanisms in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |
Izquierdo NG, Dosio GAA, Cantarero M, Luján J, Aguirrezábal LAN (2008) Weight per grain, oil concentration, and solar radiation intercepted during grain filling in black hull and striped hull sunflower hybrids. Crop Science 48, 688
| Weight per grain, oil concentration, and solar radiation intercepted during grain filling in black hull and striped hull sunflower hybrids.Crossref | GoogleScholarGoogle Scholar |
King SP, Lunn JE, Furbank RT (1997) Carbohydrate content and enzyme metabolism in developing canola siliques. Plant Physiology 114, 153–160.
| Carbohydrate content and enzyme metabolism in developing canola siliques.Crossref | GoogleScholarGoogle Scholar |
Koehler G, Wilson RC, Goodpaster JV, Sonsteby A, Lai X, Witzmann FA, You J-S, Rohloff J, Randall SK, Alsheikh M (2012) Proteomic study of low-temperature responses in strawberry cultivars (Fragaria × ananassa) that differ in cold tolerance. Plant Physiology 159, 1787–1805.
| Proteomic study of low-temperature responses in strawberry cultivars (Fragaria × ananassa) that differ in cold tolerance.Crossref | GoogleScholarGoogle Scholar |
Lancashire PD, Bleiholder H, van den Boom T, Langelüddeke P, Stauss R, Weber E, Witzenberger A (1991) A uniform decimal code for growth stages of crops and weeds. Annals of Applied Biology 119, 561–601.
| A uniform decimal code for growth stages of crops and weeds.Crossref | GoogleScholarGoogle Scholar |
Li H (2000) ‘Principles and techniques of plant physiology and biochemistry experiment.’ (Higher Education Press: Beijing)
Mandal KG, Sinha AC (2004) Nutrient management effects on light interception, photosynthesis, growth, dry-matter production and yield of Indian mustard (Brassica juncea). Journal of Agronomy & Crop Science 190, 119–129.
| Nutrient management effects on light interception, photosynthesis, growth, dry-matter production and yield of Indian mustard (Brassica juncea).Crossref | GoogleScholarGoogle Scholar |
Martin T, Oswald O, Graham IA (2002) Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: nitrogen availability. Plant Physiology 128, 472–481.
| Arabidopsis seedling growth, storage lipid mobilization, and photosynthetic gene expression are regulated by carbon: nitrogen availability.Crossref | GoogleScholarGoogle Scholar |
Minden V, Kleyer M (2011) Testing the effect-response framework: key response and effect traits determining above-ground biomass of salt marshes. Journal of Vegetation Science 22, 387–401.
| Testing the effect-response framework: key response and effect traits determining above-ground biomass of salt marshes.Crossref | GoogleScholarGoogle Scholar |
Mokhtassi-Bidgoli A, AghaAlikhani M, Nassiri-Mahallati M, Zand E, Luis Gonzalez-Andujar J, Azari A (2013) Agronomic performance, seed quality and nitrogen uptake of Descurainia sophia in response to different nitrogen rates and water regimes. Industrial Crops and Products 44, 583–592.
| Agronomic performance, seed quality and nitrogen uptake of Descurainia sophia in response to different nitrogen rates and water regimes.Crossref | GoogleScholarGoogle Scholar |
Morrison MJ (1993) Heat stress during reproduction in summer rape. Canadian Journal of Botany 71, 303–308.
| Heat stress during reproduction in summer rape.Crossref | GoogleScholarGoogle Scholar |
Norton G, Harris JF (1975) Compositional changes in developing rape seed (Brassica napus L.). Planta 123, 163–174.
| Compositional changes in developing rape seed (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |
Nunes-Nesi A, Fernie AR, Stitt M (2010) Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions. Molecular Plant 3, 973–996.
| Metabolic and signaling aspects underpinning the regulation of plant carbon nitrogen interactions.Crossref | GoogleScholarGoogle Scholar |
Pavithra HR, Gowda B, Shivanna MB (2014) Biochemical changes in the composition of developing seeds of Pongamia pinnata (L.) Pierre. Industrial Crops and Products 53, 199–208.
| Biochemical changes in the composition of developing seeds of Pongamia pinnata (L.) Pierre.Crossref | GoogleScholarGoogle Scholar |
Peng Y, Niklas KJ, Sun S (2011) The relationship between relative growth rate and whole-plant C:N:P stoichiometry in plant seedlings grown under nutrient-enriched conditions. Journal of Plant Ecology 4, 147–156.
| The relationship between relative growth rate and whole-plant C:N:P stoichiometry in plant seedlings grown under nutrient-enriched conditions.Crossref | GoogleScholarGoogle Scholar |
Rossato L, Laine P, Ourry A (2001) Nitrogen storage and remobilization in Brassica napus L. during the growth cycle: Nitrogen fluxes within the plant and changes in soluble protein patterns. Journal of Experimental Botany 52, 1655–1663.
| Nitrogen storage and remobilization in Brassica napus L. during the growth cycle: Nitrogen fluxes within the plant and changes in soluble protein patterns.Crossref | GoogleScholarGoogle Scholar |
SAS Institute (1990) ‘SAS/STAT guide for personal computers.’ (SAS Institute Inc.: Cary, NC, USA)
Schiltz S, Munier-Jolain N, Jeudy C, Burstin J, Salon C (2005) Dynamics of exogenous nitrogen partitioning and nitrogen remobilization from vegetative organs in pea revealed by 15N in vivo labeling throughout seed filling. Plant Physiology 137, 1463–1473.
| Dynamics of exogenous nitrogen partitioning and nitrogen remobilization from vegetative organs in pea revealed by 15N in vivo labeling throughout seed filling.Crossref | GoogleScholarGoogle Scholar |
Shen J, Fu T, Tu JMC (2007) Potential in production and genetic improvement of rapeseed and prospect for rape oil-based biodiesel in China. Journal of Huazhong Agricultural University 26, 894–899.
Si P, Mailer RJ, Galwey N, Turner DW (2003) Influence of genotype and environment on oil and protein concentrations of canola (Brassica napus L.) grown across southern Australia. Australian Journal of Agricultural Research 54, 397–407.
| Influence of genotype and environment on oil and protein concentrations of canola (Brassica napus L.) grown across southern Australia.Crossref | GoogleScholarGoogle Scholar |
Tan H, Yang X, Zhang F, Zheng X, Qu C, Mu J, Fu F, Li J, Guan R, Zhang H (2011) Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds. Plant Physiology 156, 1577–1588.
| Enhanced seed oil production in canola by conditional expression of Brassica napus LEAFY COTYLEDON1 and LEC1-LIKE in developing seeds.Crossref | GoogleScholarGoogle Scholar |
Tan H, Xie Q, Xiang X, Li J, Zheng S, Xu X, Guo H, Ye W (2015) Dynamic metabolic profiles and tissue-specific source effects on the metabolome of developing seeds of Brassica napus. PLoS One 10, e0124794
| Dynamic metabolic profiles and tissue-specific source effects on the metabolome of developing seeds of Brassica napus.Crossref | GoogleScholarGoogle Scholar |
Valluru R, Link J, Claupein W (2011) Natural variation and morpho-physiological traits associated with water-soluble carbohydrate concentration in wheat under different nitrogen levels. Field Crops Research 124, 104–113.
| Natural variation and morpho-physiological traits associated with water-soluble carbohydrate concentration in wheat under different nitrogen levels.Crossref | GoogleScholarGoogle Scholar |
Vigeolas H, Dongen JTV, Waldeck P, Hühn D, Geigenberger P (2003) Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape. Plant Physiology 133, 2048–2060.
| Lipid storage metabolism is limited by the prevailing low oxygen concentrations within developing seeds of oilseed rape.Crossref | GoogleScholarGoogle Scholar |
Wang H (2004) Strategy on the mid and long-term development of rapeseed variety improvement in China. Chinese Journal of Oil Crop Sciences 26, 98–101.
Wang H (2010) Review and future development of rapeseed industry in China. Chinese Journal of Oil Crop Sciences 26, 300–302.
Wang Y, Xiang L, Yu B, Hu Q, Jia Z (1997) Relationship between accumulative dynamics of seed oil content and temperature in oil sunflower. Chinese Journal of Oil Crop Sciences 19, 44–46.
White JA, Todd J, Newman T, Focks N, Girke T, de Ilárduya OM, Jaworski JG, Ohlrogge JB, Benning C (2000) A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil. Plant Physiology 124, 1582–1594.
| A new set of Arabidopsis expressed sequence tags from developing seeds. The metabolic pathway from carbohydrates to seed oil.Crossref | GoogleScholarGoogle Scholar |
