Decrement of Sugar Consumption in Rice Young Panicle Under High Temperature Aggravates Spikelet Number Reduction
These authors contributed equally to this work
Received date: 2018-11-15
Accepted date: 2019-02-08
Online published: 2019-09-30
Two rice genotypes Huanghuazhan (HHZ, heat-resistant) and IR36 (heat-susceptible) were subjected to high-temperature (HT, 40 ºC) and normal-temperature (NT, 32 ºC) treatments at the spikelet differentiation stage. HT treatment inhibited spikelet differentiation, aggravated spikelet degeneration, reduced spikelet size, and disordered carbohydrate allocation. Meanwhile, HT treatment increased nonstructural carbohydrate content in leaves, but decreased that in stems and young panicles, and the same tendencies of sucrose and starch contents were observed in leaves and stem. However, HT treatment significantly increased the sucrose content and sharply decreased the glucose and fructose contents in young panicles. Lower activity levels of soluble acid invertase (EC3.2.1.26) and sucrose synthase (EC2.4.1.13) were observed under HT treatment. Moreover, HT treatment reduced the activities of key enzymes associated with glycolysis and the tricarboxylic acid cycle, which indicated sucrose consumption was inhibited in young panicles under HT treatment. Exogenous glucose and fructose applied under HT treatment increased the spikelet number more than exogenous sucrose. In conclusion, the results demonstrated that the reduction of spikelet number under high temperature was more affected by the decrease in sugar consumption than the blocking of sucrose transport. The impairment of sucrose hydrolysis was the main reason for the inhibition of sugar utilization.
Yaliang Wang, Yikai Zhang, Qinghua Shi, Huizhe Chen, Jing Xiang, Guohui Hu, Yanhua Chen, Xiaodan Wang, Junke Wang, Zihao Yi, Defeng Zhu, Yuping Zhang . Decrement of Sugar Consumption in Rice Young Panicle Under High Temperature Aggravates Spikelet Number Reduction[J]. Rice Science, 2020 , 27(1) : 44 -55 . DOI: 10.1016/j.rsci.2019.12.005
| [1] | Bao A L, Zhao Z Q, Ding G D, Shi L, Xu F S, Cai H M.2015. The stable level ofglutamine synthetase 2 plays an important role in rice growth and in carbon-nitrogen metabolic balance. Int J Mol Sci, 16(6): 12713-12736. |
| [2] | Cao Y Y, Duan H, Yang L N, Wang Z Q, Zhou S C, Yang J C.2008. Effect of heat-stress during meiosis on grain yield of rice cultivars differing in heat-tolerance and its physiological mechanism.Acta Agron Sin, 34(12): 2134-2142. (in Chinese with English abstract) |
| [3] | Chaturvedi A K, Bahuguna R N, Shah D, Pal M, Jagadish S V K.2017. High temperature stress during flowering and grain filling offsets beneficial impact of elevated CO2 on assimilate partitioning and sink-strength in rice.Sci Rep, 7: 8227. |
| [4] | Cheng C, Zeng Y J, Cheng H H, Tan X M, Shang Q Y, Zeng Y H, Shi Q H.2019. Effects of different temperature from full heading to milking on grain filling stage on grain hormones concentrations, activities of enzymes involved in starch synthesis and accumulation in rice Nanjing 9108.Chin J Rice Sci, 33(1): 57-67. (in Chinese with English abstract) |
| [5] | Czechowski T, Bari R P, Stitt M, Scheible W R, Udvardi M K.2004. Real-time RT-PCR profiling of over 1400Arabidopsis transcription factors: Unprecedented sensitivity reveals novel root- and shoot-specific genes. Plant J, 38(2): 366-379. |
| [6] | Dubois M, Gilles K A, Hamilton J K, Rebers P A, Smith F.1956. Colorimetric method for determination of sugars and related substances.Anal Chem, 28(3): 350-356. |
| [7] | Fang X W, Tang L H, Wang Y P.2006. Selection on rice germplasm tolerant to high temperature.J Plant Genet Resour, 7(3): 342-344. (in Chinese with English abstract) |
| [8] | Glaubitz U, Erban A, Kopka J, Hincha D K, Zuther E.2015. High night temperature strongly impacts TCA cycle, amino acid and polyamine biosynthetic pathways in rice in a sensitivity- dependent manner.J Exp Bot, 66(20): 6385-6397. |
| [9] | Heng Y Q, Wu C Y, Long Y, Luo S, Ma J, Chen J, Liu J F, Zhang H, Ren Y L, Wang M, Tan J J, Zhu S S, Wang J L, Lei C L, Zhang X, Guo X P, Wang H Y, Cheng Z J, Wan J M.2018. OsALMT7 maintains panicle size and grain yield in rice by mediating malate transport. Plant Cell, 30(4): 889-906. |
| [10] | Ishibashi Y, Okamura K, Miyazaki M, Phan T, Yuasa T, Iwaya- Inoue M.2014. Expression of rice sucrose transporter geneOsSUT1 in sink and source organs shaded during grain filling may affect grain yield and quality. Environ Exp Bot, 97: 49-54. |
| [11] | Kaushal N, Awasthi R, Gupta K, Gaur P, Siddique K H M, Nayyar H.2013. Heat-stress-induced reproductive failures in chickpea (Cicer arietinum) are associated with impaired sucrose metabolism in leaves and anthers. Funct Plant Biol, 40(12): 1334-1349. |
| [12] | Li T, Liu Q H, Ohsugi R, Yamagishi T, Sasaki H.2006. Effect of high temperature on sucrose content and sucrose cleaving enzyme activity in rice grain during the filling stage.Rice Sci, 13(3): 205-210. |
| [13] | Liu X W, Meng Y L, Zhou Z G, Cao W X.2005. Dynamic characteristics of floret differentiation and degeneration in rice.Acta Agron Sin, 31(4): 451-455. (in Chinese with English abstract) |
| [14] | Matsukura C, Saitoh T, Hirose T, Ohsugi R, Perata P, Yamaguchi J.2000. Sugar uptake and transport in rice embryo: Expression of companion cell-specific sucrose transporter (OsSUT1) induced by sugar and light. Plant Physiol, 124(1): 85-93. |
| [15] | McCready R M, Guggolz J, Silviera V, Owens H S.1950. Determination of starch and amylose in vegetables.Anal Chem, 22(9): 1956-1958. |
| [16] | Miyazaki M, Araki M, Okamura K, Ishibashi Y, Yuasa T, Iwaya-Inoue M.2013. Assimilate translocation and expression of sucrose transporter,OsSUT1, contribute to high-performance ripening under heat stress in the heat-tolerant rice cultivar Genkitsukushi. J Plant Physiol, 170(18): 1579-1584. |
| [17] | Phan T T T, Ishibashi Y, Miyazaki M, Tran H T, Okamura K, Tanaka S, Nakamura J, Yuasa T, Iwaya-Inoue M.2013. High temperature-induced repression of the rice sucrose transporter (OsSUT1) and starch synthesis-related genes in sink and source organs at milky ripening stage causes chalky grains. J Agron Crop Sci, 199(3): 178-188. |
| [18] | Reid E E, Thompson P, Lyttle C R, Dennis D T.1977. Pyruvate dehydrogenase complex from higher plant mitochondria and proplastids.Plant Physiol, 59(5): 854-858. |
| [19] | Ruan Y L.2012. Signaling role of sucrose metabolism in development.Mol Plant, 5(4): 763-765. |
| [20] | Sakata T, Oshino T, Miura S, Tomabechi M, Tsunaga Y, Higashitani N, Miyazawa Y, Takahashi H, Watanabe M, Higashitani A.2010. Auxins reverse plant male sterility caused by high temperatures.Proc Natl Acad Sci USA, 107(19): 8569-8574. |
| [21] | Sanchez B, Rasmussen A, Porter J R.2014. Temperatures and the growth and development of maize and rice: A review.Global Change Biol, 20(2): 408-417. |
| [22] | Scharte J, Schön H, Tjaden Z, Weis E, Schaewen A V.2009. Isoenzyme replacement of glucose-6-phosphate dehydrogenase in the cytosol improves stress tolerance in plants.Proc Natl Acad Sci USA, 106(19): 8061-8066. |
| [23] | Scofield G N, Hirose T, Aoki N, Furbank R T.2007. Involvement of the sucrose transporter,OsSUT1, in the long-distance pathway for assimilate transport in rice. J Exp Bot, 58(12): 3155-3169. |
| [24] | Sharma K P, Sharma N.2018. Influence of high temperature on sucrose metabolism in chalky and translucent rice genotypes.Proc Natl Acad Sci India A, 88(3): 1275-1284. |
| [25] | Storme D N, Geelen D.2014. The impact of environmental stress on male reproductive development in plants: Biological processes and molecular mechanisms.Plant Cell Environ, 37(1): 1-18. |
| [26] | Suwa R, Hakata H, Hara H, El-Shemy H A, Adu-Gyamfi J, Nguyen N T, Kanai S, Lightfoot D A, Mohapatra P K, Fujita K.2010. High temperature effects on photosynthate partitioning and sugar metabolism during ear expansion in maize (Zea mays L.) genotypes. Plant Physiol Biochem, 48: 124-130. |
| [27] | van den Ende W.2014. Sugars take a central position in plant growth, development and, stress responses: A focus on apical dominance.Front Plant Sci, 5: 313. |
| [28] | Wang Y L, Zhang Y P, Zeng Y H, Wu H, Xiang J, Chen H Z, Zhang Y K, Zhu D F.2015. Effect of high temperature stress on rice spikelet differentiation and degeneration during panicle initiation stage.Chin J Agron, 36(6): 724-731. (in Chinese with English abstract) |
| [29] | Wang Y L, Zhang Y P, Zhu D F, Xiang J, Chen H Z, Zhang Y K.2016. Response of rice organ morphology and dry matter accumulation to high temperature at different panicle initiation stages.Chin J Rice Sci, 30(2): 161-169. (in Chinese with English abstract) |
| [30] | Wang Y L, Zhang Y P, Xiang J, Wang L, Chen H Z, Zhang Y K, Zhang W Q, Zhu D F.2017. Response ofindica rice spikelet differentiation and degeneration to air temperature and solar radiation of different sowing dates. Chin J Appl Ecol, 28(11): 3571-3580. (in Chinese with English abstract) |
| [31] | Wu C, Cui K H, Wang W C, Li Q, Fahad S, Hu Q Q, Huang J L, Nie L X, Peng S B.2016. Heat-induced phytohormone changes are associated with disrupted early reproductive development and reduced yield in rice.Sci Rep, 6: 34978. |
| [32] | Yu J J, Li R, Fan N L, Yang Z M, Huang B R.2017. Metabolic pathways involved in carbon dioxide enhanced heat tolerance in Bermudagrass.Front Plant Sci, 8: 1506. |
| [33] | Zeng Y H, Zhang Y P, Xiang J, Wang Y L, Chen H Z, Zhu D F.2015. Effects of low temperature on formation of spikelets and grain filling ofindica inbred rice during panicle initiation in early-season. Chin J Appl Ecol, 26(7): 2007-2014. (in Chinese with English abstract) |
| [34] | Zhang C X, Feng B H, Chen T T, Fu W M, Li H B, Li G Y, Jin Q Y, Tao L X, Fu G F.2018. Heat stress-reduced kernel weight in rice at anthesis is associated with impaired source-sink relationship and sugars allocation.Environ Exp Bot, 155: 718-733. |
| [35] | Zhang Y J.1977. Determination of glucose, fructose, sucrose and starch in fruit and vegetable with anthrone colorimetric method.Chin J Anal Chem, 5(3): 167-171. (in Chinese) |
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