Skip to main content
SpringerLink
Log in

Polyamines and ethylene in rice young panicles in response to soil drought during panicle differentiation

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

This study tested the hypothesis that polyamines (PA) and ethylene (ETH) mediate the effects of soil drought on spikelet development in rice (Oryza sativa L.). Two rice cultivars, Yong You-2640 and Yang Dao-6, with vastly different panicle sizes were grown in pots under three soil moisture treatments: well-watered (WW), moderate soil drought (MD) and severe soil drought (SD), from the onset of panicle initiation to the pollen completion stage. MD treatment significantly increased spikelet differentiation, spikelet number per panicle, fully filled grain percentage and grain yield, decreasing the percentage of degenerated spikelets, sterile spikelets and partially filled grains compared to WW treatment. In contrast, SD treatment showed opposite effects. MD also increased the contents of free spermidine (Spd), free spermine (Spm) and the ratios of free putrescine, free-Spd and free-Spm to 1-aminocylopropane-1-carboxylic acid (ACC), decreasing the ETH evolution rate and ACC content in young panicles. In contrast, SD treatment showed opposite effects. Furthermore, free-Spd and free-Spm contents increased significantly, while ETH and ACC levels, and the percentage of degenerated and sterile spikelets decreased significantly under application of Spd or an inhibitor of ETH synthesis. The results were reversed when ACC or an inhibitor of Spd and Spm synthesis was applied. These findings suggest antagonistic interactions between free-PA (Spd and Spm) and ETH in response to soil drought, mediating spikelet development in rice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

ACC :

1-aminocylopropane-1-carboxylic acid

AVG :

Aminoethoxyvinylglycine

DBH :

Days before heading

ETH :

Ethylene

MD :

Moderate soil-drought

MGBG :

Methylglyoxal-bis (guanylhydrazone)

PA :

Polyamines

Put :

Putrescine

SAM :

S-adenosyl-L-methionine

SD :

Severe soil-drought

Spd :

Spermidine

Spm :

Spermine

WW :

Well-watered

References

  • Alcazar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotech Lett 28:1867–1876

    Article  CAS  Google Scholar 

  • Alcazar R, Altabella T, Marco F, Bortalotti C, Reymond M, Koncz C, Carrasco P, Tiburcio AF (2010) Polyamines: molecules with regulatory functions in plant abiotic stress tolerance. Planta 231:1237–1249

    Article  CAS  PubMed  Google Scholar 

  • Beltrano J, Carbone A, Montaldi ER, Guiamet JJ (1994) Ethylene as promoter of wheat grain maturation and ear senescence. Plant Growth Regul 15:107–112

    Article  CAS  Google Scholar 

  • Boyer JS, Westgate ME (2004) Grain yield with limited water. J Exp Bot 55:2385–2349

    Article  CAS  PubMed  Google Scholar 

  • Chen T, Xu Y, Wang J, Wang Z, Yang J, Zhang J (2013) Polyamines and ethylene interact in rice grains in response to soil drying during grain filling. J Exp Bot 64:2523–2538

    Article  CAS  PubMed  Google Scholar 

  • Cheng CY, Lur HS (1996) Ethylene may be involved in abortion of the maize caryopsis. Physiol Plant 98:245–252

    Article  CAS  Google Scholar 

  • Davies PJ (2004) The plant hormones: their nature, occurrence and function. In: Davies PJ (ed) Plant hormones, biosynthesis, signal transduction, action! Kluwer, Dordrecht, pp 1–15

    Google Scholar 

  • Ding C, You J, Chen L, Wang S, Ding Y (2014) Nitrogen fertilizer increases spikelet number per panicle by enhancing cytokinin synthesis in rice. Plant Cell Rep 33:363–371

    Article  CAS  PubMed  Google Scholar 

  • DiTomaso JM, Shaff JE, Kochian LV (1989) Putrescine-induced wounding and its effects on membrane integrity and ion transport processes in roots of intact corn seedlings. Plant Physiol 90:988–995

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Feng H, Wang Z, Kong F, Zhang M, Zhou S (2011) Roles of carbohydrate supply and ethylene, polyamines in maize kernel set. J Integr Plant Biol 53:388–398

    Article  CAS  PubMed  Google Scholar 

  • Flores HE, Galston AW (1982) Analysis of polyamines in higher plants by high performance liquid chromatography. Plant Physiol 69:701–706

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuhrer J, Kaur-Sawhney R, Shih LM, Galston AW (1982) Effects of exogenous 1, 3-diaminopropane and spermidine on senescence of oat leaves. Plant Physiol 70:1597–1600

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gallardo M, de Rueda PM, Matilla AJ, Sánchez-Calle IM (1995) Alterations of the ethylene pathway in germinating thermo-inhibited chick-pea seeds caused by the inhibition of polyamine biosynthesis. Plant Sci 104:169–175

    Article  CAS  Google Scholar 

  • Gemperlová L, Nováková M, Vaňková R, Eder J, Cvikrová M (2006) Diurnal changes in polyamine content, arginine and ornithine decarboxylase, and diamine oxidase in tobacco leaves. J Exp Bot 57:1413–1421

    Article  PubMed  Google Scholar 

  • Goyal M, Asthir B (2010) Polyamine catabolism influences antioxidative defense mechanism in shoots and roots of five wheat genotypes under high temperature stress. Plant Growth Regul 60:13–25

    Article  CAS  Google Scholar 

  • Hou Z, Liu G, Hou L, Wang L, Liu X (2013) Regulatory function of polyamine oxidase-generated hydrogen peroxide in ethylene induced stomatal closure in Arabidopsis thaliana. J Integr Agric 12:251–262

    Article  Google Scholar 

  • Hu W, Gong H, Pua EC (2006) Modulation of SAMDC expression in Arabidopsis thaliana alters in vitro shoot organogenesis. Physiol Plant 128:740–750

    Article  CAS  Google Scholar 

  • Hummel I, Amrani AE, Gouesbet G, Hennion F, Coue´e I (2004) Involvement of polyamines in the interacting effects of low temperature and mineral supply on Pringlea antiscorbutica (Kerguelen cabbage) seedlings. J Exp Bot 55:1125–1134

    Article  CAS  PubMed  Google Scholar 

  • Jang S, Wi S, Choi Y, An G, Park K (2012) Increased polyamine biosynthesis enhances stress tolerance by preventing the accumulation of reactive oxygen species: T-DNA mutational analysis of Oryza sativa lysine decarboxylase-like protein 1. Mol Cells 34:251–262

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 5:479–485

    Article  Google Scholar 

  • Liang Y, Lur H (2002) Conjugated and free polyamine levels in normal and aborting maize kernels. Crop Sci 42:1217–1224

    Article  CAS  Google Scholar 

  • Ling Q, Su Z, Chang H, Cai J, Ho J (1983) The leaf-age model of development process in different varieties of rice. Sci Agric Sin 16: 9–18

    Google Scholar 

  • Liu H, Dong B, Zhang Y, Liu Z, Liu Y (2004) Relationship between osmotic stress and the levels of free, soluble-conjugated and insoluble-conjugated polyamines in leaves of wheat seedlings. Plant Sci 166:1261–1267

    Article  CAS  Google Scholar 

  • Liu J, Kitashiba H, Wang J, Ban Y, Moriguchi T (2007) Polyamines and their ability to provide environmental stress tolerance to plants. Plant Biotechnol 24:117–126

    Article  CAS  Google Scholar 

  • Maiale S, Sánchez DH, Guirda A, Vidal A, Ruiz O (2004) Spermine accumulation under salt stress. J Plant Physiol 161:35–42

    Article  CAS  PubMed  Google Scholar 

  • Makino A (2011) Photosynthesis, grain yield, and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129

    Article  CAS  PubMed  Google Scholar 

  • Mohapatra PK, Patel R, Sahu SK (1993) Time of flowering affects grain quality and spikelet partitioning within the rice panicle. Aust J Plant Physiol 20:231–242

    Article  Google Scholar 

  • Morgan PW, Drew MC (1997) Ethylene and plant responses to stress. Physiol Plant 100:620–630

    Article  CAS  Google Scholar 

  • Naik PK, Mohapatra PK (1999) Ethylene inhibitors promote male gametophyte survival in rice. Plant Growth Regul 28:29–39

    Article  CAS  Google Scholar 

  • Naik PK, Mohapatra PK (2000) Ethylene inhibitors enhanced sucrose synthase activity and promoted grain filling of basal rice kernels. Aust J Plant Physiol 27:997–1008

    CAS  Google Scholar 

  • Nambeesan S, AbuQamar S, Laluk K, Mattoo AK, Mickelbart MV, Ferruzzi MG, Mengiste T, Handa AK (2012) Polyamines attenuate ethylene-mediated defense responses to abrogate resistance to Botrytis cinerea in tomato. Plant Physiol 158:1034–1045

    Article  CAS  PubMed  Google Scholar 

  • Namuco OS, O’Toole JC (1986) Reproductive stage water-stress and sterility. I. Effect of stress during meiosis. Crop Sci 26:317–321

    Article  Google Scholar 

  • Narayana I, Lalonde S, Saini HS (1991) Water-stress-induced ethylene production in wheat. Plant Physiol 96:406–410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papadakis AK, Roubelakis-Angelakis KA (2005) Spatial and temporal distribution of polyamine levels and polyamine anabolism in different organs/tissues of the tobacco plant. Correlations with age, cell division/expansion, and differentiation. Plant Physiol 220:826–837

    CAS  Google Scholar 

  • Ravanel S, Gakiere B, Job D, Douce R (1998) The specific features of methionine biosynthesis, and metabolism in plants. Proc Natl Acad Sci USA 95:7805–7812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saini HS (1997) Effects of water stress on male gametophyte development in plants. Sex Plant Reprod 10:67–73

    Article  Google Scholar 

  • Saini HS, Aspinall D (1981) Effect of water deficit on sporogenesis in wheat (Triticum aestivum L.). Ann Bot 48:623–633

    Article  Google Scholar 

  • Saini HS, Westgate ME (2000) Reproductive development in grain crops during drought. Adv Agron 68:59–96

    Article  Google Scholar 

  • Sen K, Choudhuri MM, Ghosh B (1981) Changes in polyamine contents during development and germination of rice seeds. Phytochemistry 20:631–633

    Article  CAS  Google Scholar 

  • Sheoran IS, Saini HS (1996) Drought-induced male sterility in rice: changes in carbohydrate levels and enzyme activities associated with the inhibition of starch accumulation in pollen. Sex Plant Reprod 9:161–169

    Article  Google Scholar 

  • Torrigiani P, Bressanin D, Ruiz KB, Tadiello A, Trainotti L, Bonghi C, Ziosi V, Costa G (2012) Spermidine application to young developing peach fruits leads to a slowing down of ripening by impairing ripening-related ethylene and auxin metabolism and signaling. Physiol Plant 146:86–98

    Article  CAS  PubMed  Google Scholar 

  • Tsuda M, Takami S (1993) Changes of water potential in rice panicle under increasing drought stress at various stages. Jpn J Crop Sci 62:41–46

    Article  Google Scholar 

  • Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiol 113:1009–1013

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Z, Xu Y, Chen T, Zhang H, Yang J, Zhang J (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

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J (2006b) Grain filling of cereals under soil drying. New Phytol 169:223–236

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J (2010) Grain filling problem in ‘‘super’’ rice. J Exp Bot 61:1–5

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Zhang J, Liu K, Wang Z, Liu L (2006a) Abscisic acid and ethylene interact in wheat grains in response to soil drying during grain filling. New Phytol 271:293–303

    Article  Google Scholar 

  • Yang J, Zhang J, Liu K, Wang Z, Liu L (2007a) Abscisic acid and ethylene interact in rice spikelets in response to water stress during meiosis. J Plant Growth Regul 26:318–328

    Article  Google Scholar 

  • Yang J, Zhang J, Liu K, Wang Z, Liu L (2007b) Involvement of polyamines in the drought resistance of rice. J Exp Bot 58:1545–1555

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Cao Y, Zhang H, Liu L, Zhang J (2008) Involvement of polyamines in the post-anthesis development of inferior and superior spikelets in rice. Planta 228:137–149

    Article  CAS  PubMed  Google Scholar 

  • Yang W, Yin Y, Li Y, Cai T, Ni YL, Peng DL, Wang ZL (2014) Interactions between polyamines and ethylene during grain filling in wheat grown under water deficit conditions. Plant Growth Regul 72:189–201

    Article  CAS  Google Scholar 

  • Yoshida S (1976) Measurement of yield components and identification of unfertilized grains. In: Yoshida S, Forno DA, Cock JH, Gomez KA (eds) Laboratory manual for physiological studies of rice. The International Rice Research Institute, Los Baños, pp 74–78

    Google Scholar 

  • Zahedi M, Jenner CF (2003) Analysis of effects in wheat of high temperature on grain filling attributes estimated from mathematical models of grain filling. J Agric Sci 141:203–212

    Article  Google Scholar 

  • Zee SY, O’Brien TP (1970) A special type of tracheary element associated with ‘xylem discontinuity’ in the floral axis of wheat. Aust J Biol Sci 23:783–791

    Article  Google Scholar 

  • Zhang Z, Zhao H, Tang J, Li Z, Li Z, Chen D, Lin W (2014) A proteomic study on molecular mechanism of poor grain-filling of rice (Oryza sativa L.) inferior spikelets. PLoS ONE 9:e89140

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang W, Cao Z, Zhou Q, Chen J, Xu G, Gu J, Liu L, Wang Z, Yang J, Zhang H (2016) Grain filling characteristics and their relations with endogenous hormones in large- and small-grain mutants of rice. PLoS ONE 11(10):e0165321

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu G, Ye N, Yang J, Peng X, Zhang J (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 62:3907–3939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from the National Natural Science Foundation of China [Grant numbers 31461143015; 31471438], the National Key Technology Support Program of China [grant number 2014AA10A605], The National Key Research and Development Program of China [Grant number 2016YFD0300206-4], the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD), the Top Talent Supporting Program of Yangzhou University (2015-01), the Jiangsu Creation Program for Post-graduation Students [Grant number KYLX16_1398], and the Jiangsu Creation Program for Post-graduation Students [Grant number KYZZ15_0364].

Author information

Authors and Affiliations

  1. Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Yangzhou University, Yangzhou, Jiangsu, China

    Weiyang Zhang, Yingjie Chen, Zhiqin Wang & Jianchang Yang

Authors
  1. Weiyang Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yingjie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Zhiqin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jianchang Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhiqin Wang.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 21 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, W., Chen, Y., Wang, Z. et al. Polyamines and ethylene in rice young panicles in response to soil drought during panicle differentiation. Plant Growth Regul 82, 491–503 (2017). https://doi.org/10.1007/s10725-017-0275-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-017-0275-2

Keywords

Search

Navigation