Potassium deficiency aggravates yield loss in rice by restricting the translocation of non-structural carbohydrates under Sarocladium oryzae infection condition.
Journal
Physiologia plantarum
ISSN: 1399-3054
Titre abrégé: Physiol Plant
Pays: Denmark
ID NLM: 1256322
Informations de publication
Date de publication:
Nov 2019
Nov 2019
Historique:
received:
12
07
2018
revised:
27
11
2018
accepted:
03
12
2018
pubmed:
12
12
2018
medline:
6
2
2020
entrez:
12
12
2018
Statut:
ppublish
Résumé
Sheath rot disease (ShR) caused by Sarocladium oryzae (S. oryzae) infection is an emerging disease that causes severe yield loss by restricting the translocation of non-structural carbohydrates (NSC). Potassium (K) nutrition plays a critical role in disease resistance and the exportation of NSC. However, the physiological mechanisms of K with respect to ShR have not been thoroughly elucidated to date. The objectives of this study were to reveal the mechanisms by which K increases ShR resistance by regulating NSC translocation of rice, therefore, a field experiment combined with an inoculation experiment was conducted. We demonstrate that ShR disease incidence and disease index decreased dramatically with an increasing K application. K deficiency sharply induced the accumulation of NSC in the flag leaf (FL) and flag leaf sheath (FLS) under S. oryzae infection condition, which reduced the contribution of transferred NSC to final yield. A permutational multivariate analysis showed that K deficiency had a greater (49.0%, P < 0.001) effect on the NSC content variation in FL than that of S. oryzae infection (15.0%, P < 0.001). S. oryzae infection dramatically increased the difference in apparent transferred mass of NSC and cell membrane injury of diseased organs between K-deficient and K-sufficient rice. Finally, we demonstrate that cell membrane injury was a limiting factor imposed by K deficiency, which restricts the export of NSC from source organs. This work highlights the importance of K in improving ShR resistance by regulating NSC translocation (particularly the stem NSC).
Substances chimiques
Potassium
RWP5GA015D
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
352-364Subventions
Organisme : International Potash Institute Co-operation Program
Organisme : Fundamental Research Funds for the Central Universities
ID : 2662017JC010
Organisme : National Natural Science Foundation of China
ID : 31872174
Organisme : National Natural Science Foundation of China
ID : 41571284
Informations de copyright
© 2018 Scandinavian Plant Physiology Society.
Références
Ayyadurai N, Kirubakaran SI, Srisha S, Sakthivel N (2005) Biological and molecular variability of Sarocladium oryzae, the sheath rot pathogen of rice (Oryzae sativa L). Curr Microbiol 50: 319-323
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46
Amtmann A, Troufflard S, Armengaud P (2008) The effect of potassium nutrition on pest and disease resistance in plants. Physiol Plant 133: 682-691
Angay O, Fleischmann F, Recht S, Herrmann S, Matyssek R, Osswald W (2014) Sweets for the foe-effects of nonstructural carbohydrates on the susceptibility of Quercus robur against phytophthora quercina. New Phytol 203: 1282-1290
Bigirimana VP, Hua GK, Nyamangyoku OI, Höfte M (2015) Rice sheath rot: an emerging ubiquitous destructive disease complex. Front Plant Sci 6: 1066
Braun DM, Wang L, Ruan YL (2014) Understanding and manipulating sucrose phloem loading, unloading, metabolism, and signaling to enhance crop yield and food security. J Exp Bot 65: 1713-1735
Chen HJ, Wang SJ (2008) Molecular regulation of sink-source transition in rice leaf sheaths during the heading period. Acta Physiol Plant 30: 639-649
Cakmak I, Hengeler C, Marschner H (1994) Changes in phloem export of sucrose in leaves in response to phosphorus, potassium and magnesium deficiency in bean plants. J Exp Bot 45: 1251-1257
Chen LQ (2014) Sweet sugar transporters for phloem transport and pathogen nutrition. New Phytol 201: 1150-1155
Fu J, Huang Z, Wang Z, Yang J, Zhang J (2011) Pre-anthesis non-structural carbohydrate reserve in the stem enhances the sink strength of inferior spikelets during grain filling of rice. Field Crop Res 123: 170-182
Ghosh MK, Amudha R, Jayachandran S, Sakthivel N (2002) Detection and quantification of phytotoxic metabolites of Sarocladium oryzae, in sheath rot-infected grains of rice. Lett Appl Microbiol 34: 398-401
Gerardeaux E, Jordan-Meille L (2009) Effect of carbon assimilation on dry weight production and partitioning during vegetative growth. Plant Soil 324: 329-343
Gerardeaux E, Jordan-Meille L, Constantin J, Pellerin S, Dingkuhn M (2010) Changes in plant morphology and dry matter partitioning caused by potassium deficiency in Gossypium hirsutum, L. Environ Exp Bot 67: 451-459
Gil L, Yaron I, Shalitin D, Sauer N, Turgeon R, Wolf S (2011) Sucrose transporter plays a role in phloem loading in cmv-infected melon plants that are defined as symplastic loaders. Plant J 66: 366-374
Hu W, Loka DA, Fitzsimons TR, Zhou Z, Oosterhuis DM (2018) Potassium deficiency limits reproductive success by altering carbohydrate and protein balances in cotton (Gossypium hirsutum L.). Environ Exp Bot 145: 87-94
Hu W, Coomer TD, Loka DA, Oosterhuis DM, Zhou Z (2017) Potassium deficiency affects the carbon-nitrogen balance in cotton leaves. Plant Physiol Biochem 115: 408-417
Hittalmani S, Mahesh HB, Mahadevaiah C (2016) De novo genome assembly and annotation of rice sheath rot fungus Sarocladium oryzae reveals genes involved in helvolic acid and cerulenin biosynthesis pathways. BMC Genomics 17: 271
Hodges DM, Delong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207: 604-611
Hu W, Yang J, Meng Y, Wang Y, Chen B, Zhao W, Oosterhuis DM, Zhou Z (2015) Potassium application affects carbohydrate metabolism in the leaf subtending the cotton (Gossypium hirsutum, L.) boll and its relationship with boll biomass. Field Crop Res 179: 120-131
Jönsson U (2006) A conceptual model for the development of phytophthora disease in Quercus robur. New Phytol 171: 55-68
Kanai S, Ohkura K, Adu-Gyamfi JJ, Mohapatra PK, Nguyen NT, Saneoka H, Fujita K (2007) Depression of sink activity precedes the inhibition of biomass production in tomato plants subjected to potassium deficiency stress. J Exp Bot 58: 2917-2928
Kühn C, Grof CP (2010) Sucrose transporters of higher plants. Curr Opin Plant Biol 13: 287-297
Lecompte F, Nicot PC, Ripoll J, Abro MA, Raimbault AK, Lopezlauri F, Bertin N (2017) Reduced susceptibility of tomato stem to the necrotrophic fungus botrytis cinerea is associated with a specific adjustment of fructose content in the host sugar pool. Ann Bot 119: 931-943
Li G, Pan J, Cui K, Yuan M, Hu Q, Wang W, Mohapatra P, Nie L, Huang J, Peng S (2017) Limitation of unloading in the developing grains is a possible cause responsible for low stem non-structural carbohydrate translocation and poor grain yield formation in rice through verification of recombinant inbred lines. Front Plant Sci 8: 1369
Marschner P (2012) Marschner's Mineral Nutrition of Higher Plants. Academic Press, London, pp 178-189
Moscatello S, Proietti S, Buonaurio R, Famiani F, Raggi V, Walker RP, Battistelli A (2017) Peach leaf curl disease shifts sugar metabolism in severely infected leaves from source to sink. Plant Physiol Biochem 112: 9-18
Mfernanda D, Anthonyf VH, Scottc C (2009) Grain number and grain weight in wheat lines contrasting for stem water soluble carbohydrate concentration. Field Crop Res 112: 43-54
Morita S, Nakano H (2011) Nonstructural carbohydrate content in the stem at full heading contributes to high performance of ripening in heat-tolerant rice cultivar Nikomaru. Crop Sci 51: 818-828
Oosterhuis DM, Loka DA, Raper TB (2013) Potassium and stress alleviation: physiological functions and management of cotton. J Plant Nutr Soil Sci 176: 331-343
Prabhu AS, Fageria NK, Huber DM (2007) Potassium nutrition and plant diseases. In: Datnoff LE, Elmer WH, Huber DM (eds) Mineral Nutrition and Plant Disease. The American Phytopathological Society Press, Saint Paul
Pan Y, Lu Z, Lu J, Li X, Cong R, Ren T (2017) Effects of low sink demand on leaf photosynthesis under potassium deficiency. Plant Physiol Biochem 113: 110-121
Pan J, Cui K, Dong W, Huang J, Xiang J, Nie L (2011) Relationships of non-structural carbohydrates accumulation and translocation with yield formation in rice recombinant inbred lines under two nitrogen levels. Physiol Plant 141: 321
Terao T, Nagata K, Morino K, Hirose T (2010) A gene controlling the number of primary rachis branches also controls the vascular bundle formation and hence is responsible to increase the harvest index and grain yield in rice. Theor Appl Genet 120: 875-893
Sakthivel N (2001) Sheath rot disease of rice: current status and control strategies. In: Major Fungal Diseases of Rice. Springer, Dordrecht, pp 271-283
Saravanakumar D, Lavanya N, Muthumeena K, Raguchander T, Samiyappan R (2009) Fluorescent pseudomonad mixtures mediate disease resistance in rice plants against sheath rot (Sarocladium oryzae) disease. BioControl 54: 273-286
Sun Y, Wang M, Li Y, Gu Z, Ling N, Shen Q, Guo S (2017) Wilted cucumber plants infected by Fusarium oxysporum f. sp. cucumerinum do not suffer from water shortage. Ann Bot 120: 427
Sakthivel N, Amudha R, Muthukrishnan S (2002) Production of phytotoxic metabolites by Sarocladium oryzae. Mycol Res 106: 609-614
Voegele RT, Mendgen K (2003) Rust haustoria: nutrient uptake and beyond [review]. New Phytol 159: 93-100
Wang DR, Han R, Wolfrum EJ, Mccouch SR (2017) The buffering capacity of stems: genetic architecture of nonstructural carbohydrates in cultivated asian rice, Oryza sativa. New Phytol 215: 658-671
Walters DR, Bingham IJ (2007) Influence of nutrition on disease development caused by fungal pathogens: implications for plant disease control. Ann Appl Biol 151: 307-324
Wu W, Shah F, Shah F, Huang J (2015) Rice sheath blight evaluation as affected by fertilization rate and planting density. Austral Plant Pathol 44: 183-189
Wang M, Sun Y, Sun G, Liu X, Zhai L, Shen Q, Guo S (2015a) Water balance altered in cucumber plants infected with Fusarium oxysporum f. sp. cucumerinum. Sci Rep 5: 7722
Wang M, Zheng Q, Shen Q, Guo S (2013) The critical role of potassium in plant stress response. Int J Mol Sci 14: 7370-7390
Wang L, Lu Q, Wen X, Lu C (2015b) Enhanced sucrose loading improves rice yield by increasing grain size. Plant Physiol 169: 2848-2862
Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory Manual for Physiological Studies of Rice. International Rice Research Institute Press, Manila
Yan SL, Lehrer AT, Hajirezaei MR, Springer A, Komor E (2008) Modulation of carbohydrate metabolism and chloroplast structure in sugarcane leaves which were infected by sugarcane yellow leaf virus (scylv). Physiol Mol Plant Pathol 73: 78-87
Yang J, Zhang J, Wang Z, Zhu Q, Wei W (2001) Remobilization of carbon reserves in response to water deficit during grain filling of rice. Field Crop Res 71: 47-55
Zou J, Lu JW, Li YS, Li XK (2011) Regional evaluation of winter rapeseed response to K fertilization, K use efficiency, and critical level of soil K in the Yangtze River valley. Agric Sci China 10: 911-920
Zahoor R, Dong H, Abid M, Zhao W, Wang Y, Zhou Z (2017) Potassium fertilizer improves drought stress alleviation potential in cotton by enhancing photosynthesis and carbohydrate metabolism. Environ Exp Bot 137: 73-83
Zhang XZ (1992) Methods for Physiology Research in Crops. Agriculture Press, Beijing