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Interactions between polyamines and ethylene during grain filling in wheat grown under water deficit conditions

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Abstract

This study was to test the hypothesis that polyamines (PAs) and ethylene may be involved in mediating the effect of water deficit on grain filling. Two wheat cultivars, drought-tolerant Shannong16 (SN16) and drought-sensitive Jimai22 (JM22), were used and subjected to well-watered and severe water deficit (SD) during grain filling. SD reduced the weight of superior and inferior grains, by 7.38 and 23.54 % in JM22, 13.8 and 2.2 % in SN16, respectively. Higher free-spermidine (Spd) and free-spermine (Spm) concentration and lower free-putrescine (Put) concentration, ethylene evolution rate (EER) and 1-aminocylopropane-1-carboxylic acid (ACC) concentration were found in superior grains than those in inferior ones. Opposite to the variations of Spd and Spm concentration, ACC, Put concentration and EER were significantly increased under SD. The percentage variation of PAs and ACC differed with cultivars and grain types. ACC concentration of superior and inferior grains under SD increased significantly at 21 days post-anthesis, by 90 and 164 % in JM22, 65 and 13.2 % in SN16, respectively. The equivalent value of Put concentration was 1.04 and 7.9 % in JM22, 34.4 and 10.3 % in SN16. Spd concentration of superior grains showed a higher decrease than that of inferior ones in both cultivars, while Spm exhibited an opposite trend between both grain types. These percentage variations were highly consistent with the differed responses of weight of both grain types to SD in JM22 and SN16. Grain filling rate was negatively correlated with EER and ACC concentration, while positively correlated with Spd and Spm concentration as well as the ratio of Spd or Spm to ACC. Exogenous Spd or aminoethoxyvinylglycine (an inhibitor of ethylene synthesis by inhibiting ACC synthesis) obviously reduced ACC concentration and EER and increased Spd and Spm concentration, while exogenous ethephon (an ethylene-releasing agent) or methylglyoxal-bis (an inhibitor of Spd and Spm synthesis) showed the opposite effects. The results suggested that it would be good for wheat to have the physiological traits of higher Spd and Spm, as well as a higher Spd/ACC or Spm/ACC, under SD.

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Abbreviations

ACC:

1-Aminocylopropane-1-carboxylic acid

AVG:

Aminoethoxyvinylglycine

DPA:

Days post-anthesis

EER:

Ethylene evolution rate

FID:

Flame ionization detector

GS13:

Growth stages (3 leaves unfolded)

GS31:

Growth stages (1st node visible)

MGBG:

Methylglyoxal-bis(guanylhydrazone)

PA(s):

Polyamine (s)

Put:

Putrescine

SAM:

S-adenosyl-l-methionine

Spd:

Spermidine

Spm:

Spermine

SD:

Severe water deficit

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. Biotechnol Lett 28:1867–1876

    Article  CAS  PubMed  Google Scholar 

  • Barnabas B, Jager K, Feher A (2008) The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ 31(1):11–38

    CAS  PubMed  Google Scholar 

  • Beltrano J, Ronco MG, Montaldi ER (1999) Drought stress syndrome in wheat is provoked ethylene evolution imbalance and reversed by rewatering, aminoethoxyvinylglycine, or sodium benzoate. J Plant Growth Regul 18:59–64

    Article  CAS  PubMed  Google Scholar 

  • Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125

    Article  CAS  Google Scholar 

  • Bray EA (2002) Abscisic acid regulation of gene expression during water-deficit stress in the era of the Arabidopsis genome. Plant Cell Environ 25:153–161

    Article  CAS  PubMed  Google Scholar 

  • Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914

    Article  CAS  PubMed  Google 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 64:2523–2538

    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 

  • 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 Central  PubMed  Google Scholar 

  • Duan HG, Yuan S, Liu WJ, Xi DH, Qing DH, liang HG, Lin HH (2006) Effects of exogenous spermidine on photosystem II of wheat seedlings under water stress. J Integr Plant Biol 48(8):920–927

    Article  CAS  Google Scholar 

  • Feng HY, Wang ZM, Kong FN, Zhang MJ, Zhou SL (2011) Roles of carbohydrate supply and ethylene, polyamines in maize kernel set. J Integr Plant Biol 53(5):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 Central  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 

  • Hu WW, 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, Couee 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 

  • Jiang MY, Zhang JH (2004) Abscisic acid and antioxidant defense in plant cells. Acta Bot Sin 46(1):1–9

    CAS  Google Scholar 

  • Jiang D, Cao W, Dai T, Jing Q (2003) Activities of key enzymes for starch synthesis in relation to growth of superior and inferior grains on winter wheat (Triticum aestivum L.) spike. Plant Growth Regul 41:247–257

    Article  CAS  Google Scholar 

  • Jones HG, Corlett JE (1992) Current topics in drought physiology: review. J Agric Sci 119:291–296

    Article  Google Scholar 

  • Lee TM (1997) Polyamine regulation of growth and chilling tolerance of rice (Oryza sativa L.) roots cultured in vitro. Plant Sci 122:111–117

    Article  CAS  Google Scholar 

  • Li B, Sang T, He LZ, Sun J, Li J, Guo SR (2013) Exogenous spermidine inhibits ethylene production in leaves of cucumber seedlings under NaCl stress. J Am Soc Hortic Sci 138:108–113

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Liu JH, 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 

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

    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(11):997–1008

    CAS  Google Scholar 

  • Naik BI, Srivastava SK (1978) Effect of polyamines on tissue permeability. Biochemistry 17:1885–1887

    CAS  Google Scholar 

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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005a) Sites and regulation of polyamine catabolism in the tobacco plant. Correlations with cell division/expansion, cell cycle progression, and vascular development. Plant Physiol 138:2174–2184

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Paschalidis KA, Roubelakis-Angelakis KA (2005b) 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 138(1):142–152

    Article  CAS  PubMed Central  PubMed  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  Google Scholar 

  • Richards FJ (1959) A flexible growth function for empirical use. J Exp Bot 10:290–301

    Article  Google Scholar 

  • Sharp RE (2002) Interaction with ethylene: changing views on the role of abscisic acid in root and shoot growth responses to water stress. Plant Cell Environ 25:211–222

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Yin Y, He M, Zhang Y, Lu S, Li Q, Shi S (2003) Allocation of photosynthates and grain growth of two wheat cultivars with different potential grain growth in response to pre- and post-anthesis shading. J Agron Crop Sci 189:280–285

    Article  Google Scholar 

  • Wang ZQ, Xu YJ, Wang JC, Yang JC, Zhang JH (2012) Polyamine and ethylene interactions in grain filling of superior and inferior spikelets of rice. Plant Growth Regul 66:215–228

    Article  CAS  Google Scholar 

  • Yang JC, Zhang JH, Ye YX, Wang ZQ, Zhu QS, Liu LJ (2004) Involvement of abscisic acid and ethylene in the responses of rice grains to water stress during filling. Plant Cell Environ 27:1055–1064

    Article  CAS  Google Scholar 

  • Yang JC, Zhang JH, Liu K, Wang ZQ, Liu LJ (2006) Abscisic acid and ethylene interact in wheat grains in response to soil drying during grain filling. New Phytol 171(2):293–303

    Article  CAS  PubMed  Google Scholar 

  • Yang JC, Cao YY, Zhang H, Liu LJ, Zhang JH (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 

  • Zadoks JC, Chang TT, Konzak CF (1974) A decimal code for the growth stages of cereals. Weed Res 14:415–421

    Article  Google Scholar 

  • Zhao FG, Sun C, Liu YL, Zhang WH (2003) Relationship between polyamine metabolism in roots and salt tolerance of barley seedlings. Acta Bot Sin 45:295–300

    CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the support of the the National Natural Science Foundation of China (No. 31271661, 30871477), the Shandong Modern Agricultural Technology and Industry System. The National Basic Research Program of China (973 Program, No. 2009CB118602), the Special Fund for Agro-scientific Research in the Public Interest of China (No. 201203100, 201203029) and the National Science and Technology Support Program of China (No. 2012BAD04B05).

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  1. National Key Laboratory of Crop Biology, Ministry of Science and Technology, Shandong Agricultural University, Tai’an, 271018, Shandong, People’s Republic of China

    Weibing Yang, Yanping Yin, Yong Li, Tie Cai, Yingli Ni, Dianliang Peng & Zhenlin Wang

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  1. Weibing Yang
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Correspondence to Zhenlin Wang.

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Yang, W., Yin, Y., Li, Y. et al. Interactions between polyamines and ethylene during grain filling in wheat grown under water deficit conditions. Plant Growth Regul 72, 189–201 (2014). https://doi.org/10.1007/s10725-013-9851-2

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