Hostname: page-component-586b7cd67f-gb8f7 Total loading time: 0 Render date: 2024-11-28T04:16:04.423Z Has data issue: false hasContentIssue false
  • English
  • Français

Rapid endosperm development promotes early maturity in weedy rice (Oryza sativa f. spontanea)

Published online by Cambridge University Press:  24 March 2020

Can Zhao ,
Wenrong Xu ,
Lingchao Meng ,
Sheng Qiang ,
Weimin Dai ,
Zheng Zhang  and
Xiaoling Song Open the ORCID record for Xiaoling Song [Opens in a new window]
Can Zhao
Affiliation:
Ph.D Student, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Wenrong Xu
Affiliation:
Master’s Student, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Lingchao Meng
Affiliation:
Master’s Student, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Sheng Qiang
Affiliation:
Professor, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Weimin Dai
Affiliation:
Associate Professor, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Zheng Zhang
Affiliation:
Postdoctoral Research Associate, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
Xiaoling Song*
Affiliation:
Professor, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China
*
Author for correspondence: Xiaoling Song, Weed Research Laboratory, College of Life Sciences, Nanjing Agricultural University, Nanjing210095, Jiangsu, P. R. China. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Early maturity allows weedy rice (Oryza sativa L. f. spontanea) to persist by escaping harvest in paddy fields. A shorter grain-filling period contributes to the early maturity of weedy rice. However, the differences in morphology and endosperm development in the caryopsis between weedy and cultivated rice are largely unexplored. Here, we selected four biotypes of weedy rice and associated cultivated rice (ACR; Oryza sativa) from different latitudes to conduct a common garden experiment. The endosperm development process of the caryopsis was observed by optical microscopy and electron microscopy. Endosperm cell division and starch accumulation rate during grain filling were also measured. The grain development progress in weedy rice was more rapid and earlier than that in ACR. The endosperm development progress of weedy rice was 6 to 8 d earlier than that of ACR. The endosperm cells of weedy rice cellularized earlier and more rapidly than those of ACR, and the starch grains of weedy rice were more sharply polygonal and compactly arranged than those of ACR. The active endosperm cell division period in weedy rice was 4 to 7 d shorter than that in ACR, while the active starch accumulation period of weedy rice was 2 to 8 d shorter than that of ACR. The rapid development of endosperm cells and starch grains leads to the shorter grain-filling period of weedy rice. weedy rice.

Keywords

Weedy ricecultivated riceendosperm cell divisionstarch accumulationearly maturity
Type
Research Article
Information
Weed Science , Volume 68 , Issue 2 , March 2020 , pp. 168 - 178
Copyright
© Weed Science Society of America, 2020

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Associate Editor: Steven S. Seefeldt, Washington State University

*

These authors contributed equally to this work.

References

Ahmed, N, Tetlow, IJ, Nawaz, S, Iqbal, A, Mubin, M, Rehman, MSN, Butt, A, Lightfoot, DA, Maekawa, M (2015) Effect of high temperature on grain filling period, yield, amylose content and activity of starch biosynthesis enzymes in endosperm of basmati rice. J Sci Food Agric 95:2237–2243CrossRefGoogle ScholarPubMed
Akasaka, M, Konishi, S, Izawa, T, Ushiki, J (2011) Histological and genetic characteristics associated with the seed-shattering habit of weedy rice (Oryza sativa L.) from Okayama, Japan. Breeding Sci 61:168–173CrossRefGoogle Scholar
Becraft, PW (2001) Cell fate specification in the cereal endosperm. Semin Cell Dev Biol 12:387394CrossRefGoogle ScholarPubMed
Bevilacqua, CB, Basu, S, Pereira, A, Tseng, TM, Zimmer, PD, Burgos, NR (2015) Analysis of stress-responsive gene expression in cultivated and weedy rice differing in cold stress tolerance. PLoS ONE 10:e0132100CrossRefGoogle ScholarPubMed
Bhagiraths, C, Davide, J (2010) Weedy rice (Oryza sativa) I. Grain characteristics and growth response to competition of weedy rice variants from five Asian countries. Weed Sci 58:374–380Google Scholar
Birch, CPD (1999) A new generalized logistic sigmoid growth equation compared with the Richards growth equation. Ann Bot 83:713–723CrossRefGoogle Scholar
Burgos, NR, Norman, RJ, Gealy, DR, Black, H (2006) Competitive N uptake between rice and weedy rice. Field Crops Res 99:96–105CrossRefGoogle Scholar
Chen, TT, Xu, YJ, Wang, JC, Wang, ZQ, Yang, JC, Zhang, JH (2013) Polyamines and ethylene interact in rice grains in response to soil drying during grain filling. J Exp Bot 64:2523–2538CrossRefGoogle ScholarPubMed
Chen, YF, Gu, YJ, Wang, Z (2009) Difference in caryopsis development among four rice varieties differing in grain weight. Chin J Rice Sci 23:405–413Google Scholar
Dai, L, Dai, WM, Song, XL, Lu, BR, Qiang, S (2014) A comparative study of competitiveness between different genotypes of weedy rice (Oryza sativa) and cultivated rice. Pest Manag Sci 70:113–122CrossRefGoogle ScholarPubMed
Dai, L, Song, XL, He, BY, Valverde, BE, Qiang, S (2017) Enhanced photosynthesis endows seedling growth vigor contributing to the competitive dominance of weedy rice over cultivated rice. Pest Manag Sci 73:1410–1420CrossRefGoogle Scholar
Delouche, JC, Burgos, NR, Gealy, DR, de San Martin, GZ, Labrada, R, Larinde, M, Rosell, C (2007) Weedy Rices: Origin, Biology, Ecology and Control. FAO Plant Production and Protection Paper 188. Rome: FAO. Pp 3–15Google Scholar
Ding, GH, Liu, XL, Ma, DR, Wang, XX, Yang, G, Gao, MC, Gao, Q, Sun, J, Chen, WF (2013) Responses of weedy rice to drought stress at germination and seedling stages. Appl Mech Mater 317:451–459CrossRefGoogle Scholar
Ding, Y (1961) Rice Cultivation Science in China. Beijing: Beijing Agriculture Press. Pp 512–517Google Scholar
Dong, MH, Xie, YL, Qiao, ZY, Liu, XB, Wu, XY, Zhao, BH, Yang, JC (2011) Variation in carbohydrate and protein accumulation between spikelets at different positions within a rice panicle during grain filling. Chin J Rice Sci 25:297306Google Scholar
Gealy, DR, Saldain, NE, Talbert, RE (2000) Emergence of red rice (Oryza sativa) ecotypes under dry-seeded rice (Oryza sativa) culture. Weed Technol l14:406–412CrossRefGoogle Scholar
Gu, XY, Foley, ME (2003) Multiple loci and epistases control genetic variation for seed dormancy in weedy rice (Oryza sativa). Genetics 166:1503–1516CrossRefGoogle Scholar
Gu, XY, Foley, ME, Horvath, DP, Anderson, JV, Feng, JH, Zhang, LH, Mowry, CR, Ye, H, Suttle, JC, Kadowaki, K, Chen, ZX (2011) Association between seed dormancy and pericarp color is controlled by a pleiotropic gene that regulates abscisic acid and flavonoid synthesis in weedy red rice. Genetics 189:1515–1524CrossRefGoogle ScholarPubMed
Guo, LA, Hu, YG, Yang, GT, Yan, SM, Yi, J (2014) The research on the accumulation of grain starch and change of related enzymes activity in rice with different amylose contents. J Yunnan 36:942–949Google Scholar
Hannah, L, James, M (2008) The complexities of starch biosynthesis in cereal endosperms. Curr Opin Biotechnol 19:160–165CrossRefGoogle ScholarPubMed
James, MG, Denyer, K, Myers, AM. (2003) Starch synthesis in the cereal endosperm. Curr Opin Plant Biol 6:215–222CrossRefGoogle ScholarPubMed
Jiang, H, Hu, ZZ (2013) Determination of amylose and amylopectin content in indica rice by dual-wavelength spectrophotometry. Cereal Feed Ind 12:22–25Google Scholar
Jing, FU, Xu, YJ, Lu, C, Yuan, LM, Wang, ZQ, Yang, JC (2013) Changes in enzyme activities involved in starch synthesis and hormone concentrations in superior and inferior spikelets and their association with grain filling of super rice. Rice Sci 2:120–128Google Scholar
Kanapeckas, KL, Tseng, TM, Vigueira, CC, Ortiz, A, Bridges, WC, Burgos, NR, Fischer, AJ, Lawton-Rauh, A (2018) Contrasting patterns of variation in weedy traits and unique crop features in divergent populations of US weedy rice (Oryza sativa sp.) in Arkansas and California. Pest Manag Sci 74:1404–1415CrossRefGoogle ScholarPubMed
Kim, J, Shon, J, Lee, CK, Yang, W, Yoon, Y, Yang, WH, Kim, YG, Lee, BW (2011) Relationship between grain filling duration and leaf senescence of temperate rice under high temperature. Field Crop Res 122:207–213CrossRefGoogle Scholar
Kuk, YI, Guh, JO, Chon, SU (1997) Difference of classification, growth and herbicidal tolerance in collected weedy rice (Oryza sativa). Korean J Weed Sci 17:31–43Google Scholar
Li, DL, Li, XG, Gu, YJ, Wang, Z (2014) Investigation of endosperm cell development of different rice varieties. Chin J Rice Sci 19:3757–3768Google Scholar
Li, XM, Zhao, WC, Zhou, XX, Feng, JP, Gao, YJ, Yao, XH, Liu, Y, Liu, J, Yang, R, Zhao, FK, Wang, SH (2017) The use of toluidine blue staining combined with paraffin sectioning and the optimization of freeze-thaw counting methods for analysing root-knot nematodes in tomato. Hortic Environ Biotechnol 58:620–626CrossRefGoogle Scholar
Liu, DT, Yu, XR, Zhu, DM, Liu, J, Zhang, X, Gao, DR (2017) Relationship between caryopsis microstructure and endogenous auxin level and the fast grain filling of Yangmai 16. J Trit Crops 37:739–749Google Scholar
Liu, Z, Wang, Z, Zhu, J (2016) Observational studies on amyloplasts with single-starch granule in rice endosperm. Braz J Bot 39:1–12CrossRefGoogle Scholar
Londo, JP, Schaal, BA (2007) Origins and population genetics of weedy red rice in the USA. Mol Ecol 16:4523–4535CrossRefGoogle ScholarPubMed
Morita, S, Yonemaru, JI, Takanashi, J (2005) Grain growth and endosperm cell size under high night temperatures in rice (Oryza sativa L.). Ann Bot 95:695–701CrossRefGoogle Scholar
Nayyar, H, Kaur, G, Kumar, S, Upadhyaya, HD (2007) Low temperature effects during seed filling on chickpea genotypes (Cicer arietinum L.): probing mechanisms affecting seed reserves and yield. J Agron Crop Sci 193:336–344CrossRefGoogle Scholar
Nunes, AL, Delatorre, CA, Merotto, A Jr (2014) Gene expression related to seed shattering and the cell wall in cultivated and weedy rice. Plant Biol 16:888–896CrossRefGoogle ScholarPubMed
Panda, BB, Badoghar, AK, Sekhar, S, Shaw, BP, Mohapatra, PK (2016) 1-MCP treatment enhanced expression of genes controlling endosperm cell division and starch biosynthesis for improvement of grain filling in a dense-panicle rice cultivar. Plant Sci 246:11–25CrossRefGoogle Scholar
Richards, FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–301CrossRefGoogle Scholar
Shao, J, Dai, WM, Zhang, LJ, Qiang, S (2011) Genetic diversity and origin of weedy rice in Jiangsu province, China. Acta Agron Sin 37:1324–1332CrossRefGoogle Scholar
Tang, T, Lv, B, Liang, JS (2009) Comparison of grain filling characteristics of various rice varieties. J Yangzhou Univ Agric Life Sci Ed 30:78–83Google Scholar
Thurber, CS, Hepler, PK, Caicedo, AL (2011) Timing is everything: early degradation of abscission layer is associated with increased seed shattering in U.S. weedy rice. BMC Plant Biol 11:14–23CrossRefGoogle ScholarPubMed
Thurber, CS, Michael, R, Gross, BL, Olsen, KM, Jia, Y, Caicedo, AL (2010) Molecular evolution of shattering loci in U.S. weedy rice. Mol Ecol 19:3271–3284CrossRefGoogle ScholarPubMed
Wang, Z, Gu, Y, Hirasawa, T, Ookawa, T, Yanahara, S (2004) Comparison of caryopsis development between two rice varieties with remarkable difference in grain weights. Acta Bot Sin 46:698–710Google Scholar
Wang, Z, Gu, YJ, Zheng, YK (2012) Structure observation of rice endosperm cell development and its mineral element analysis. Chin J Rice Sci 26:693–705Google Scholar
Wang, ZQ, Xu, YJ, Chen, TT, Zhang, H, Yang, JC, Zhang, JH (2015) Abscisic acid and the key enzymes and genes in sucrose-to-starch conversion in rice spikelets in response to soil drying during grain filling. Planta 241:1091–1107CrossRefGoogle ScholarPubMed
Wei, CX, Lan, SY, Xu, ZX (2002) Ultrastructural features of nucleus degradation during programmed cell death of starchy endosperm cells in rice. Acta Bot Sin 44:1396–1402Google Scholar
Wu, XB, Liu, JX, Li, DQ, Liu, CM (2016) Rice caryopsis development: dynamic changes in the endosperm. J Integr Plant Biol 58:786–798CrossRefGoogle ScholarPubMed
Xia, HB, Wang, W, Xia, H, Zhao, W, Lu, BR (2011) Conspecific crop-weed introgression influences evolution of weedy rice (Oryza sativa f. spontanea) across a geographical range. PLoS ONE 6:e16189CrossRefGoogle ScholarPubMed
Xiong, F, Wang, Z, Cheng, G, Wang, J (2015) Caryopsis development and main quality characteristics in different indica rice varieties. Rice Sci 12:238–242Google Scholar
Xu, XM, Li, G, Su, Y, Wang, XL (2018) Effect of weedy rice at different densities on photosynthetic characteristics and yield of cultivated rice. Photosynthetica 56:520–526CrossRefGoogle Scholar
Yang, JC, Zhang, JH, Wang, ZQ, Zhu, QS, Wang, W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323CrossRefGoogle ScholarPubMed
Yoshida, S (1981) Fundamentals of Rice Crop Science. Volume 22. Los Banos, Manila: International Rice Research Institute. 59 pGoogle Scholar
Yu, XR, Zhou, L, Xiong, F, Wang, Z (2014) Structural and histochemical characterization of developing rice caryopsis. Rice Sci 21:142–149CrossRefGoogle Scholar
Zhang, J, Burgos, NR, Kun, MA, Zhou, YJ, Geng, RM, Yu, LQ (2008) Genetic diversity and relationship of weedy rice in Taizhou city, Jiangsu province, China. Rice Sci 15:295–302CrossRefGoogle Scholar
Zhang, LJ, Dai, WM, Wu, CR, Song, XL, Qiang, S (2012) Genetic diversity and origin of Japonica- and Indica-like rice biotypes of weedy rice in the Guangdong and Liaoning provinces of China. Genet Resour Crop Evol 59:399–410CrossRefGoogle Scholar
Zhang, ZJ, Wang, ZQ, Xu, S, Lang, YZ, Cao, XZ, Zhu, QS (1998a) Studies on relation between proliferation and filling of endosperm cells and the change of physiological activity of fertilized ovary. Acta Agron Sin 24:670–676Google Scholar
Zhang, ZJ, Wang, ZQ, Zhu, QS (1998b) Proliferation of endosperm cell and its relation to the growth of grain in rice. Acta Agron Sin 24:257–264Google Scholar
Zhao, C, Xu, WR, Song, XL, Dai, WM, Dai, L, Zhang, Z, Qiang, S (2018) Early flowering and rapid grain filling determine early maturity and escape from harvesting in weedy rice. Pest Manag Sci 74:465–476CrossRefGoogle ScholarPubMed
Zheng, YK, Wang, Z (2015) The cereal starch endosperm development and its relationship with other endosperm tissues and embryo. Protoplasm 252:33–40CrossRefGoogle ScholarPubMed
Zheng, YK, Zeng, DE, Wei, HP, Xu, Y, Gu, YJ, Wang, Z (2017) Structure observation of rice endosperm tissue. Chin J Rice Sci 31:91–98Google Scholar
Zhu, GH, Ye, NH, Yang, JC, Peng, XX, Zhang, JH (2011) Regulation of expression of starch synthesis genes by ethylene and ABA in relation to the development of rice inferior and superior spikelets. J Exp Bot 62:3907–3916CrossRefGoogle ScholarPubMed
Zhu, QS, Cao, XZ, Luo, YQ (1988) Growth analysis in the process of grain filling in rice. Acta Agron Sin 14:182–192Google Scholar
Ziska, LH, Gealy, DR, Burgos, N, Caicedo, AL, Gressel, J, Lawton-Rauh, AL, Avila, LA, Theisen, G, Norsworthy, J, Ferrero, A, Vidotto, F, Johnson, DE, Ferreira, FG, Marchesan, E, Menezes, V, Cohn, MA, Linscombe, S, Carmona, L, Tang, R and Merotto, A (2015) Weedy (red) rice: an emerging constraint to global rice production. Adv Agron 129:181–228CrossRefGoogle Scholar
Supplementary material: File

Zhao et al. supplementary material

Tables S1-S3 and Figure S1

Download Zhao et al. supplementary material(File)
File 67.3 KB