Plant Growth Regulation

, Volume 86, Issue 2, pp 263–271 | Cite as

The involvement of long non-coding RNAs in the formation of high temperature-induced grain chalkiness in rice

  • Rongjian Luo
  • Ruijie Cao
  • Guiai Jiao
  • Yusong Lv
  • Min Zhong
  • Shaoqing Tang
  • Xiangjin WeiEmail author
  • Peisong HuEmail author
Original paper


A period of exposure to high ambient temperatures can damage the process of grain filling in rice, potentially inducing the endosperm to become chalky. Given the established involvement of long non-coding RNAs (lncRNAs) in regulating plant development and its stress response, the purpose here was to reveal the extent to which lncRNA activity contributes to the endosperm chalkiness syndrome. Among 578 lncRNAs identified in spikelets harvested ten days after fertilization from plants exposed to high temperature stress, 14 were found to be significantly up-regulated expressed than in control plants, while 45 were significantly down-regulated expressed. Of these 59 differentially expressed lncRNAs, 32 were predicted as interacting with five mRNAs involved in starch metabolism and catabolism, indicating an involvement of these lncRNAs in starch formation in the endosperm, and hence in causing the chalkiness syndrome.


Long non-coding RNA (lncRNA) High temperature Chalkiness Starch metabolism Rice 



This work was supported by the National Key Research and Development Program of China (2016YFD0101801), the National S&T Major Project of China (2016ZX08001006), and by the Central level, non-profit, scientific research institutes basic R and D operations Special Fund (Y2017PT46; 2017RG002-1).

Author contributions

RL, RC and GJ performed the experiments. RL and XW analyzed the data. PH and XW designed the project. RL and XW draft the manuscript. YL, MZ, and ST performed a critical revision of the article. All authors read and approved the final manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare no conflict of interest.

Supplementary material

10725_2018_426_MOESM1_ESM.pdf (475 kb)
Supplementary material 1 (PDF 475 KB)
10725_2018_426_MOESM2_ESM.xlsx (335 kb)
Supplementary material 2 (XLSX 334 KB)


  1. Bari R, Datt Pant B, Stitt M, Scheible WR (2006) PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol 141:988–999CrossRefPubMedPubMedCentralGoogle Scholar
  2. Chen LL (2016) Linking long noncoding RNA localization and function. Trends Biochem Sci 41:761–772CrossRefPubMedGoogle Scholar
  3. Chiou TJ, Aung K, Lin SI, Wu CC, Chiang SF, Su CL (2006) Regulation of phosphate homeostasis by microRNA in Arabidopsis. Plant Cell 18:412–421CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chung PJ, Jung H, Jeong DH, Ha SH, Choi YD, Kim JK (2016) Transcriptome profiling of drought responsive noncoding RNAs and their target genes in rice. BMC Genom 17:563CrossRefGoogle Scholar
  5. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676CrossRefGoogle Scholar
  6. Dai X, Zhao PX (2011) psRNATarget: a plant small RNA target analysis server. Nucleic Acids Res 39:W155–W159CrossRefPubMedPubMedCentralGoogle Scholar
  7. Ding J, Lu Q, Ouyang Y, Mao H, Zhang P, Yao J, Xu C, Li X, Xiao J, Zhang Q (2012) A long noncoding RNA regulates photoperiod-sensitive male sterility, an essential component of hybrid rice. Proc Natl Acad Sci USA 109:2654–2659CrossRefPubMedGoogle Scholar
  8. Fatica A, Bozzoni I (2014) Long non-coding RNAs: new players in cell differentiation and development. Nat Rev Genet 15:7–21CrossRefGoogle Scholar
  9. Fitzgerald MA, McCouch SR, Hall RD (2009) Not just a grain of rice: the quest for quality. Trends Plant Sci 14:133–139CrossRefPubMedGoogle Scholar
  10. Franco-Zorrilla JM, Valli A, Todesco M, Mateos I, Puga MI, Rubio-Somoza I, Leyva A, Weigel D, Garcia JA, Paz-Ares J (2007) Target mimicry provides a new mechanism for regulation of microRNA activity. Nat Genet 39:1033–1037CrossRefGoogle Scholar
  11. Guebel DV, Nudel BC, Giulietti AM (1991) A simple and rapid micro-Kjeldahl method for total nitrogen analysis. Biotechnol Tech 5:427–430CrossRefGoogle Scholar
  12. Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902CrossRefPubMedPubMedCentralGoogle Scholar
  13. Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299CrossRefPubMedGoogle Scholar
  14. Kong L, Zhang Y, Ye ZQ, Liu XQ, Zhao SQ, Wei L, Gao G (2007) CPC: assess the protein-coding potential of transcripts using sequence features and support vector machine. Nucleic Acids Res 35:W345–W349CrossRefPubMedPubMedCentralGoogle Scholar
  15. Lin SI, Santi C, Jobet E, Lacut E, El Kholti N, Karlowski WM, Verdeil JL, Breitler JC, Perin C, Ko SS, Guiderdoni E, Chiou TJ, Echeverria M (2010) Complex regulation of two target genes encoding SPX-MFS proteins by rice miR827 in response to phosphate starvation. Plant Cell Physiol 51:2119–2131CrossRefPubMedGoogle Scholar
  16. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 3′ processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327:94–97CrossRefPubMedGoogle Scholar
  17. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402–408CrossRefGoogle Scholar
  18. Miyahara K, Wada T, Sonoda JY, Tsukaguchi T, Miyazaki M, Tsubone M, Yamaguchi O, Ishibashi M, Iwasawa N, Umemoto T, Kondo M (2017) Detection and validation of QTLs for milky-white grains caused by high temperature during the ripening period in Japonica rice. Breed Sci 67:333–339CrossRefPubMedPubMedCentralGoogle Scholar
  19. Nakata M, Fukamatsu Y, Miyashita T, Hakata M, Kimura R, Nakata Y, Kuroda M, Yamaguchi T, Yamakawa H (2017) High temperature-induced expression of rice alpha-amylases in developing endosperm produces chalky grains. Front Plant Sci 8:2089CrossRefPubMedPubMedCentralGoogle Scholar
  20. Ohdan T, Francisco PB Jr, Sawada T, Hirose T, Terao T, Satoh H, Nakamura Y (2005) Expression profiling of genes involved in starch synthesis in sink and source organs of rice. J Exp Bot 56:3229–3244CrossRefPubMedGoogle Scholar
  21. Qin T, Zhao H, Cui P, Albesher N, Xiong L (2017) A nucleus-localized long non-coding RNA enhances drought and salt stress tolerance. Plant Physiol 175:1321–1336CrossRefPubMedPubMedCentralGoogle Scholar
  22. Shin SJ, Ahn H, Jung I, Rhee S, Kim S, Kwon HB (2016) Novel drought-responsive regulatory coding and non-coding transcripts from Oryza Sativa L. Genes Genom 38:949–960CrossRefGoogle Scholar
  23. Siebenmorgen TJ, Grigg BC, Lanning SB (2013) Impacts of preharvest factors during kernel development on rice quality and functionality. Annu Rev Food Sci T 4:101–115CrossRefGoogle Scholar
  24. Sreenivasulu N, Butardo VM Jr, Misra G, Cuevas RP, Anacleto R, Kavi Kishor PB (2015) Designing climate-resilient rice with ideal grain quality suited for high-temperature stress. J Exp Bot 66:1737–1748CrossRefPubMedPubMedCentralGoogle Scholar
  25. Sun L, Luo H, Bu D, Zhao G, Yu K, Zhang C, Liu Y, Chen R, Zhao Y (2013) Utilizing sequence intrinsic composition to classify protein-coding and long non-coding transcripts. Nucleic Acids Res 41:e166CrossRefPubMedPubMedCentralGoogle Scholar
  26. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis polycomb target. Nature 462:799–802CrossRefPubMedGoogle Scholar
  27. Tashiro TWIF (1989) A comparison of the effect of high temperature on grain development in wheat and rice. Ann Bot 64:59–65CrossRefGoogle Scholar
  28. Tashiro TWIF (1991a) The effect of high temperature on kernel dimensions and the type and occurrence of kernel damage in rice. Aust J Agric Res 42:485–496CrossRefGoogle Scholar
  29. Tashiro TWIF (1991b) The effect of high temperature on the accumulation of dry matter, carbon and nitrogen in the kernel of rice. Aust J Plant Physiol 18:259–265CrossRefGoogle Scholar
  30. Thitisaksakul M, Jiménez RC, Arias MC, Beckles DM (2012) Effects of environmental factors on cereal starch biosynthesis and composition. J Cereal Sci 56:67–80CrossRefGoogle Scholar
  31. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, Salzberg SL, Wold BJ, Pachter L (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 28:511–515CrossRefPubMedPubMedCentralGoogle Scholar
  32. Ulitsky I, Bartel DP (2013) lincRNAs: genomics, evolution, and mechanisms. Cell 154:26–46CrossRefPubMedPubMedCentralGoogle Scholar
  33. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43:904–914CrossRefPubMedPubMedCentralGoogle Scholar
  34. Wang Z, Hu H, Huang H, Duan K, Wu Z, Wu P (2009) Regulation of OsSPX1 and OsSPX3 on expression of OsSPX domain genes and Pi-starvation signaling in rice. J Integr Plant Biol 51:663–674CrossRefPubMedGoogle Scholar
  35. Wang Y, Fan X, Lin F, He G, Terzaghi W, Zhu D, Deng XW (2014) Arabidopsis noncoding RNA mediates control of photomorphogenesis by red light. Proc Natl Acad Sci USA 111:10359–10364CrossRefGoogle Scholar
  36. Wang H, Niu QW, Wu HW, Liu J, Ye J, Yu N, Chua NH (2015a) Analysis of non-coding transcriptome in rice and maize uncovers roles of conserved lncRNAs associated with agriculture traits. Plant J 84:404–416CrossRefPubMedGoogle Scholar
  37. Wang J, Yu W, Yang Y, Li X, Chen T, Liu T, Ma N, Yang X, Liu R, Zhang B (2015b) Genome-wide analysis of tomato long non-coding RNAs and identification as endogenous target mimic for microRNA in response to TYLCV infection. Sci Rep 5:16946CrossRefPubMedPubMedCentralGoogle Scholar
  38. Wang J, Meng X, Dobrovolskaya OB, Orlov YL, Chen M (2017) Non-coding RNAs and their toles in stress response in plants. Genom Proteom Bioinform 15:301–312CrossRefPubMedPubMedCentralGoogle Scholar
  39. Wei X, Jiao G, Lin H, Sheng Z, Shao G, Xie L, Tang S, Xu Q, Hu P (2017) GRAIN INCOMPLETE FILLING 2 regulates grain filling and starch synthesis during rice caryopsis development. J Integr Plant Biol 59:134–153CrossRefPubMedGoogle Scholar
  40. Wu HJ, Wang ZM, Wang M, Wang XJ (2013) Wide-spread long non-coding RNAs (lncRNAs) as endogenous target mimics (eTMs) for microRNAs in plants. Plant Physiol 161:1875–1884CrossRefPubMedPubMedCentralGoogle Scholar
  41. Wu X, Liu J, Li D, Liu CM (2016) Rice caryopsis development II: dynamic changes in the endosperm. J Integr Plant Biol 58:786–798CrossRefPubMedGoogle Scholar
  42. Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37:916–930CrossRefPubMedGoogle Scholar
  43. Yamakawa H, Hirose T, Kuroda M, Yamaguchi T (2007) Comprehensive expression profiling of rice grain filling-related genes under high temperature using DNA microarray. Plant Physiol 144:258–277CrossRefPubMedPubMedCentralGoogle Scholar
  44. Yue R, Lu C, Qi J, Han X, Yan S, Guo S, Liu L, Fu X, Chen N, Yin H, Chi H, Tie S (2016) Transcriptome analysis of cadmium-treated roots in maize (Zea mays L.). Front Plant Sci 7:1298PubMedPubMedCentralGoogle Scholar
  45. Zhang YC, Liao JY, Li ZY, Yu Y, Zhang JP, Li QF, Qu LH, Shu WS, Chen YQ (2014) Genome-wide screening and functional analysis identify a large number of long noncoding RNAs involved in the sexual reproduction of rice. Genome Biol 15:512CrossRefPubMedPubMedCentralGoogle Scholar
  46. Zhou Y, Xu Z, Duan C, Chen Y, Meng Q, Wu J, Hao Z, Wang Z, Li M, Yong H, Zhang D, Zhang S, Weng J, Li X (2016) Dual transcriptome analysis reveals insights into the response to Rice black-streaked dwarf virus in maize. J Exp Bot 67:4593–4609CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Rongjian Luo
    • 1
  • Ruijie Cao
    • 1
  • Guiai Jiao
    • 1
  • Yusong Lv
    • 1
  • Min Zhong
    • 1
  • Shaoqing Tang
    • 1
  • Xiangjin Wei
    • 1
    Email author
  • Peisong Hu
    • 1
    Email author
  1. 1.State Key Laboratory of Rice BiologyChina National Rice Research InstituteHangzhouPeople’s Republic of China

Personalised recommendations