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Cleistogamous spike and chasmogamous spike carbon remobilization improve the seed potential yield of Cleistogenes songorica under water stress

Published online by Cambridge University Press:  27 April 2022

Zhengshe Zhang ,
Mengjie Bai ,
Qibo Tao ,
Fan Wu ,
Qi Yan ,
Zhibiao Nan ,
Yanrong Wang  and
Jiyu Zhang Open the ORCID record for Jiyu Zhang [Opens in a new window]
Zhengshe Zhang
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China College of Ecology, Lanzhou University, Lanzhou 730000, China
Mengjie Bai
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Qibo Tao
Affiliation:
College of Grassland Science, Qingdao Agricultural University, Qingdao 266109, China
Fan Wu
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Qi Yan
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Zhibiao Nan
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Yanrong Wang
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
Jiyu Zhang*
Affiliation:
State Key Laboratory of Grassland Agro-ecosystems, Key Laboratory of Grassland Livestock Industry Innovation, Ministry of Agriculture and Rural Affairs, Engineering Research Center of Grassland Industry, Ministry of Education, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou 730020, China
*
*Author for Correspondence: Jiyu Zhang, E-mail: [email protected]
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Abstract

Developmental signals and environmental stresses regulate carbon distribution in the vegetative and reproductive organs of plants and affect seed yield. Cleistogenes songorica is a xerophytic grass with great potential application value in ecological restoration. However, how carbohydrate transport and distribution during grain filling affect the seed yield of C. songorica under water stress is not clear. The present study showed that the soluble sugar and starch contents of cleistogamous (CL) spikes and chasmogamous (CH) spikes were significantly higher at the milk stage, which was attributed to a significantly higher seed number and seed yield per spike under water stress conditions than under well-watered conditions (P < 0.01). RNA-seq data revealed a total of 54,525 differentially expressed genes (DEGs) under water stress conditions, but only 3744 DEGs were shared among all comparison groups. Weighted gene co-expression network analysis showed that the transport and distribution of carbohydrates were regulated by ABA-responsive genes (CsABA8OX1_1, CsABA8OX1_2, CsABA8OX2_1, CsABA8OX2_2, CsNCED3, CsNCED1_1, CsNCED1_2 and CsNCED4_1) and sugar transport and starch synthesis genes (CsSUS1, CsSUS2, CsSUS3, CsAGP1, CsAGP4, CsAGP5, CsSSS1 and CsSBE5) under water stress conditions. These genes jointly regulated carbohydrate remobilization in sources (stems, leaves and sheaths) to promote grain filling and improve seed yield. The present study helped to clarify the phenotypic, metabolic and transcriptional response mechanisms of vegetative organs, such as stems and leaves, and reproductive organs, such as CL spikes and CH spikes, to promote carbohydrate redistribution under water stress, and it provides theoretical guidance for improving seed yields.

Keywords

carbonCleistogenes songoricaseed yield water stressstarch synthesis genes
Type
Research Paper
Information
Seed Science Research , Volume 32 , Issue 1 , March 2022 , pp. 34 - 45
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Copyright
Copyright © The Author(s), 2022. Published by Cambridge University Press

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References

Aoki, N, Hirose, T, Scofield, GN, Whitfeld, PR and Furbank, RT (2003) The sucrose transporter gene family in rice. Plant and Cell Physiology 44, 223–232.CrossRefGoogle ScholarPubMed
Chen, HJ and Wang, SJ (2008) Molecular regulation of sink-source transition in rice leaf sheaths during the heading period. Acta Physiologiae Plantarum 30, 639–649.CrossRefGoogle Scholar
Chen, HJ and Wang, SJ (2012) Abscisic acid enhances starch degradation and sugar transport in rice upper leaf sheaths at the post-heading stage. Acta Physiologiae Plantarum 34, 1493–1500.CrossRefGoogle Scholar
Chen, LQ, Hou, BH, Lalonde, S, Takanaga, H, Hartung, ML, Qu, XQ, Guo, WJ, Kim, JG, Underwood, W, Chaudhuri, B, Chermak, D, Antony, G, White, FF, Somerville, SC, Mudgett, MB and Frommer, WB (2010) Sugar transporters for intercellular exchange and nutrition of pathogens. Nature 468, 527–532.CrossRefGoogle ScholarPubMed
Chen, LQ, Lin, IW, Qu, XQ, Sosso, D, McFarlane, HE, Londoño, A, Samuels, AL and Frommer, WB (2015) A cascade of sequentially expressed sucrose transporters in the seed coat and endosperm provides nutrition for the Arabidopsis embryo. The Plant Cell 27, 607–619.CrossRefGoogle ScholarPubMed
Dong, T, Park, Y and Hwang, I (2015) Abscisic acid: biosynthesis, inactivation, homoeostasis and signalling. Essays in Biochemistry 58, 29–48.Google ScholarPubMed
Du, H, Wu, N, Chang, Y, Li, XH, Xiao, JH and Xiong, LZ (2013) Carotenoid deficiency impairs ABA and IAA biosynthesis and differentially affects drought and cold tolerance in rice. Plant Molecular Biology 83, 475–488.CrossRefGoogle ScholarPubMed
Durand, M, Mainson, D, Porcheron, B, Maurousset, L, Lemoine, R and Pourtau, N (2018) Carbon source-sink relationship in Arabidopsis thaliana: the role of sucrose transporters. Planta 247, 587–611.CrossRefGoogle ScholarPubMed
Eom, J, Chen, L, Sosso, D, Julius, BT, Lin, IW, Qu, X, Braun, DM and Frommer, WB (2015) SWEETs, transporters for intracellular and intercellular sugar translocation. Current Opinion in Plant Biology 25, 53–62.CrossRefGoogle ScholarPubMed
Fan, XR, Jia, LJ, Li, YL, Smith, SJ, Miller, AJ and Shen, QR (2007) Comparing nitrate storage and remobilization in two rice cultivars that differ in their nitrogen use efficiency. Journal of Experimental Botany 58, 1729–1740.CrossRefGoogle ScholarPubMed
Fischer, RA (2008) The importance of grain or kernel number in wheat: a reply to Sinclair and Jamieson. Field Crops Research 105, 15–21.CrossRefGoogle Scholar
Fischer, RA (2011) Wheat physiology: a review of recent developments. Crop and Pasture Science 62, 95–114.CrossRefGoogle Scholar
Ghanem, ME, Albacete, A, Smigocki, AC, Frébort, I, Pospíšilová, H, Martínez-Andújar, C, Acosta, M, Sánchez-Bravo, J, Lutts, S, Dodd, IC and Pérez-Alfocea, F (2011) Root-synthesized cytokinins improve shoot growth and fruit yield in salinized tomato (Solanum lycopersicum L.) plants. Journal of Experimental Botany 62, 125–140.CrossRefGoogle ScholarPubMed
González, FG, Miralles, DJ and Slafer, GA (2011) Wheat floret survival as related to pre-anthesis spike growth. Journal of Experimental Botany 62, 4889–4901.CrossRefGoogle ScholarPubMed
Kirby, EJM (1988) Analysis of leaf, stem and ear growth in wheat from terminal spikelet stage to anthesis. Field Crops Research 18, 127–140.CrossRefGoogle Scholar
Li, GH, Pan, JF, Cui, KH, Yuan, MS, Hu, QQ, Wang, WC, Mohapatra, PK, Nie, LX, Huang, JL and Peng, SB (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. Frontiers in Plant Science 8, 1369.CrossRefGoogle ScholarPubMed
Li, XY, 2015. Turfgrass management techniques and seed yield sustainability of Cleistogenes songoriga. PhD thesis, Lanzhou University, Lanzhou, 86 pp.Google Scholar
Li, XY, Wang, YR, Wei, X, Tai, JH, Jia, CZ, Hu, XW and Trethewey, JAK (2014) Planting density and irrigation timing affects Cleistogenes songorica seed yield sustainability. Agronomy Journal 106, 1690–1696.CrossRefGoogle Scholar
Li, W, Sun, K, Ren, ZY, Song, CX, Pei, XY, Liu, YG, Wang, ZY, He, KL, Zhang, F, Zhou, XJ, Ma, XF and Yang, DG (2018) Molecular evolution and stress and phytohormone responsiveness of SUT genes in Gossypium hirsutum. Frontiers in Genetics 9, 494.CrossRefGoogle ScholarPubMed
Lipiec, J, Doussan, C, Nosalewicz, A and Kondracka, K (2013) Effect of drought and heat stresses on plant growth and yield: a review. International Agrophysics 27, 463–477.CrossRefGoogle Scholar
Mao, XZ, Cai, T, Olyarchuk, JG and Wei, LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21, 3787–3793.CrossRefGoogle Scholar
Mohammadi, MH S, Etemadi, N, Arab, MM, Aalifar, M, Arab, M and Pessarakli, M (2017) Molecular and physiological responses of Iranian perennial ryegrass as affected by trinexapac ethyl, paclobutrazol and abscisic acid under drought stress. Plant Physiology and Biochemistry 111, 129–143.CrossRefGoogle Scholar
Muvunyi, B, Yan, Q, Wu, F, Min, XY, Yan, ZZ, Kanzana, G, Wang, YR and Zhang, JY (2018) Mining Late Embryogenesis Abundant (LEA) family genes in Cleistogenes songorica, a xerophyte perennial desert plant. International Journal of Molecular Sciences 19, 3430.CrossRefGoogle ScholarPubMed
Niu, XL and Nan, ZB (2017) Roots of Cleistogenes songorica improved soil aggregate cohesion and enhance soil water erosion resistance in rainfall simulation experiments. Water Air Soil Pollution 228, 109.CrossRefGoogle Scholar
Panigrahi, R, Kariali, E, Panda, BB, Lafarge, T and Mohapatra, PK (2019) Corrigendum to: controlling the trade-off between spikelet number and grain filling: the hierarchy of starch synthesis in spikelets of rice panicle in relation to hormone dynamics. Functional Plant Biology 46, 595.CrossRefGoogle ScholarPubMed
Ruan, YL, Patrick, JW, Bouzayen, M, Osorio, S and Fernie, AR (2012) Molecular regulation of seed and fruit set. Trends in Plant Science 17, 656–665.CrossRefGoogle ScholarPubMed
Scofield, GN, Hirose, T, Gaudron, JA, Furbank, RT, Upadhyaya, NM and Ohsugi, R (2002) Antisense suppression of the rice transporter gene, OsSUT1, leads to impaired grain filling and germination but does not affect photosynthesis. Functional Plant Biology 29, 815–826.CrossRefGoogle Scholar
Tao, QB, Lv, YY, Mo, Q, Bai, MJ, Han, YH and Wang, YR (2018) Impacts of priming on seed germination and seedling emergence of Cleistogenes songorica under drought stress. Seed Science and Technology 46, 239–257.CrossRefGoogle Scholar
Tao, QB, Bai, MJ, Jia, CZ, Han, YH and Wang, YR (2021) Effects of irrigation and nitrogen fertilization on seed yield, yield components, and water use efficiency of Cleistogenes songorica. Agronomy 11, 466.CrossRefGoogle Scholar
Vallabhaneni, R and Wurtzel, ET (2010) From epoxycarotenoids to ABA: the role of ABA 8’-hydroxylases in drought-stressed maize roots. Archives of Biochemistry and Biophysics 504, 112–117.CrossRefGoogle ScholarPubMed
Wang, GQ and Zhang, JH (2020) Carbohydrate, hormone and enzyme regulations of rice grain filling under post-anthesis soil drying. Environmental and Experimental Botany 178, 104165.CrossRefGoogle Scholar
Wang, ZQ, Xu, YJ, Chen, TT, Zhang, H, Yang, JC and 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, 1091–1107.CrossRefGoogle ScholarPubMed
Wang, GQ, Hao, SS, Gao, B, Chen, MX, Liu, YG, Yang, JC, Ye, NH and Zhang, JH (2017) Regulation of gene expression in the remobilization of carbon reserves in rice stems during grain filling. Plant and Cell Physiology 58, 1391–1404.CrossRefGoogle ScholarPubMed
Wang, GQ, Li, HX, Feng, L, Chen, MX, Meng, SA, Ye, NH and Zhang, JH (2019a) Transcriptomic analysis of grain filling in rice inferior grains under moderate soil drying. Journal of Experimental Botany 70, 1597–1611.CrossRefGoogle Scholar
Wang, GQ, Li, HX, Wang, K, Yang, JC, Duan, MJ, Zhang, JH and Ye, NH (2019b) Regulation of gene expression involved in the remobilization of rice straw carbon reserves results from moderate soil drying during grain filling. The Plant Journal 101, 604–618.CrossRefGoogle Scholar
Wang, GQ, Li, HX, Gong, YL, Yang, JC, Yi, YK, Zhang, JH and Ye, NH (2020) Expression profile of the carbon reserve remobilization from the source to sink in rice in response to soil drying during grain filling. Food and Energy Security 9, e204.CrossRefGoogle Scholar
Wu, F, Zhang, DY, Muvunyi, BP, Yan, Q, Zhang, YF, Yan, ZZ, Cao, MS, Wang, YR and Zhang, JY (2018) Analysis of microRNA reveals cleistogamous and chasmogamous floret divergence in dimorphic plant. Scientific Reports 8, 6287.CrossRefGoogle ScholarPubMed
Xue, GP, McIntyre, CL, Jenkins, CLD, Glassop, D, van Herwaarden, AF and Shorter, R (2008) Molecular dissection of variation in carbohydrate metabolism related to water-soluble carbohydrate accumulation in stems of wheat. Plant Physiology 146, 441–454.CrossRefGoogle ScholarPubMed
Yan, Q, Wu, F, Yan, ZZ, Li, J, Ma, TT, Zhang, YF, Zhao, YF, Wang, YR and Zhang, JY (2019) Differential co-expression networks of long non-coding RNAs and mRNAs in Cleistogenes songorica under water stress and during recovery. BMC Plant Biology 19, 23.CrossRefGoogle ScholarPubMed
Yang, J, Luo, DP, Yang, B, Frommer, WB and Eom, J (2018) SWEET11 and 15 as key players in seed filling in rice. New Phytologist 218, 604–615.CrossRefGoogle ScholarPubMed
Zhang, JY, John, UP, Wang, YR, Li, X, Gunawardana, D, Polotnianka, RM, Spangenberg, GC and Nan, ZB (2011) Targeted mining of drought stress-responsive genes from EST resources in Cleistogenes songorica. Journal of Plant Physiology 168, 1844–1851.CrossRefGoogle ScholarPubMed
Zhang, Z, Huang, J, Gao, YM, Liu, Y, Li, JP, Zhou, XN, Yao, CS, Wang, ZM, Sun, ZC and Zhang, YH (2020) Suppressed ABA signal transduction promotes sucrose utility in stem and reduces grain number in wheat under water stress. Journal of Experimental Botany 71, 7241–7256.CrossRefGoogle Scholar
Zhang, Z, Li, J, Hu, NY, Li, W, Qin, WL, Li, JP, Gao, YM, Liu, Y, Sun, ZC, Yu, K, Wang, ZM and Zhang, YH (2021a) Spike growth affects spike fertility through the number of florets with green anthers before floret abortion in wheat. Field Crops Research 260, 108007.CrossRefGoogle Scholar
Zhang, JY, Wu, F, Yan, Q, John, UP, Cao, MS, Xu, P, Zhang, ZS, Ma, TT, Zong, XF, Li, J, Liu, RJ, Zhang, YF, Zhao, YF, Kanzana, G, Lv, YY, Nan, ZB, Spangenberg, G and Wang, YR (2021b) The genome of Cleistogenes songorica provides a blueprint for functional dissection of dimorphic flower differentiation and drought adaptability. Plant Biotechnology Journal 19, 532–547.CrossRefGoogle Scholar
Zong, XF, Yan, Q, Wu, F, Ma, Q and Zhang, JY (2020) Genome-wide analysis of the role of NAC family in flower development and abiotic stress responses in Cleistogenes songorica. Genes 11, 927.CrossRefGoogle ScholarPubMed
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