Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Signal transduction during wheat grain development

Abstract

Main conclusion

This review examines the signaling pathways from the developmental and environmental point of view and the interactions among external conditions, hormonal regulations, and sugarsensing in wheat.

Grain development is the key phase of reproductive growth that is closely associated with vegetative organ senescence, initiation of grain filling, pre-stored assimilates remobilization, and maturation. Senescence is characterized by loss of chlorophyll and the degradation of proteins, nucleic acids, lipids as well as nutrient exports to the sink. The initiation and progression of vegetative organ senescence are under the control of an array of environmental signals (such as biotic and abiotic stresses, darkness, and nutrient availability) and endogenous factors (including aging, multiple hormones, and sugar availability). This review will discuss the major breakthroughs in signal transduction for the wheat (Triticum aestivum) grain development achieved in the past several years, with focuses on the regulation of senescence, reserves remobilization and biosynthesis of main components of the grain. Different mechanisms of diverse signals in controlling different phrases of wheat grain development, and cross talks between different signaling pathways will also be discussed. For perspectives, key signaling networks for grain development remain to be elucidated, including cross talks and the interactions between various environmental factors and internal signals.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Aguera E, Cabello P, de la Haba P (2010) Induction of leaf senescence by low N nutrition in sunflower (Helianthus annuus) plants. Physiol Plant 138(3):256–267

  2. Assmann SM (2005) G proteins go green: a plant G protein signaling FAQ sheet. Science 310:71–73

  3. Bazargani MM, Sarhadi E, Bushehri AAS, Matros A, Mock HP, Naghavi MR, Hajihoseini V, Mardi M, Hajirezaei MR, Moradi F, Ehdaie B, Salekdeh GH (2011) A proteomics view on the role of drought-induced senescence and oxidative stress defense in enhanced stem reserves remobilization in wheat. J Proteomics 74:1959–1973

  4. Buchanan-Wollaston V (1997) The molecular biology of leaf senescence. J Exp Bot 48:181–199

  5. Buchanan-Wollaston V, Earl S, Harrison E, Mathas E, Navabpour S, Page T, Pink D (2003) The molecular analysis of leaf senescence – a genomics approach. Plant Biotechnol J 1:3–22

  6. Capron D, Mouzeyar S, Boulaflous A, Girousse C, Rustenholz C, Laugier C, Paux E, Bouzidi MF (2012) Transcriptional profile analysis of E3 ligase and hormone-related genes expressed during wheat grain development. BMC Plant Biol 12:35

  7. Chauhan S, Srivalli S, Nautiyal AR, Khanna-Chopra R (2009) Wheat cultivars differing in heat tolerance show a differential response to monocarpic senescence under high temperature stress and the involvement of serine proteases. Photosynthetica 47(4):536–547

  8. Chen F, Li Q, Sun L, He Z (2006) The rice 14-3-3 gene family and its involvement in responses to biotic and abiotic stress. DNA Res 13:53–63

  9. Chen Z, Huang J, Muttucumaru N, Powers SJ, Halford NG (2013) Expression analysis of abscisic acid (ABA) and metabolic signaling factors in developing endosperm and embryo of barley. J Cereal Sci 58:255–262

  10. Coello P, Hirano E, Hey SJ, Muttucumaru N, Martínez-Barajas E, Parry MAJ, Halford NG (2012) Evidence that abscisic acid promotes degradation of SNF1-related protein kinase (SnRK) 1 in wheat and activation of a putative calcium dependent SnRK2. J Exp Bot 63:913–924

  11. Comparot S, Lingiah G, Martin T (2003) Function and specificity of 14-3-3 proteins in the regulation of carbohydrate and nitrogen metabolism. J Exp Bot 54:595–604

  12. Crafts-Brandner SJ, Hölzer R, Feller U (1998) Influence of nitrogen deficiency on senescence and the amounts of RNA and proteins in wheat leaves. Physiol Plant 102:192–200

  13. Criado MV, Roberts IN, Echeverria M, Barneix AJ (2007) Plant growth regulators and induction of leaf senescence in nitrogen-deprived wheat plants. J Plant Growth Regul 26:301–307

  14. Criado MV, Caputo C, Roberts IN, Castro MA, Barneix AJ (2009) Cytokinin-induced changes of nitrogen remobilization and chloroplast ultrastructure in wheat (Triticum aestivum). J Plant Physiol 166:1775–1785

  15. Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679

  16. d’Aloisio E, Paolacci AR, Dhanapal AP, Tanzarella OA, Porceddu E, Ciaffi MR (2010) The protein disulfide isomerase gene family in bread wheat (T. aestivum L.). BMC Plant Biol 10:101

  17. Derkx AP, Orford S, Griffiths S, Foulkes MJ, Hawkesford MJ (2012) Identification of differentially senescing mutants of wheat and impacts on yield, biomass and nitrogen partitioning(f). J Integr Plant Biol 54(8):555–566

  18. Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annu Rev Plant Biol 53:203–224

  19. Fu H, Subramanian RR, Masters SC (2000) 14-3-3 proteins: structure, function, and regulation. Annu Rev Pharmacol 40:617–647

  20. Fulgosi H, Soll J, Maraschin SD, Korthout HAAJ, Wang M, Testerink C (2002) 14-3-3 proteins and plant development. Plant MolBiol 50:1019–1029

  21. Gallé Á, Csiszár J, Secenji M, Guóth A, Cseuz L, Tari I, Györgyey J, Erdei L (2009) Glutathione transferase activity and expression patterns during grain filling in flag leaves of wheat genotypes differing in drought tolerance: response to water deficit. J Plant Physiol 166:1878–1891

  22. Gan S, Amasino RM (1997) Making sense of senescence. Molecular genetic regulation and manipulation of leaf senescence. Plant Physiol 113:313–319

  23. Ge P, Ma C, Wang S, Gao L, Li X, Guo G, Ma W, Yan Y (2012) Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal BioanalChem 402:1297–1313

  24. Govind G, Seiler C, Wobus U, Sreenivasulu N (2011) Importance of ABA homeostasis under terminal drought stress in regulating grain filling events. Plant Signal Behav 6:1228–1231

  25. Guitman MR, Arnozis PA, Barneix AJ (1991) Effect of source–sink relations and nitrogen nutrition on senescence and N remobilization in the flag leaf of wheat. Physiol Plant 82:278–284

  26. Guo G, Lv D, Yan X, Subburaj S, Ge P, Li X, Hu Y, Yan Y (2012) Proteome characterization of developing grains in bread wheat cultivars (Triticum aestivum L.). BMC Plant Biol 12:147

  27. Hess JR, Carman JG, Banowetz GM (2002) Hormones in wheat kernels during embryony. J Plant Physiol 159:379–386

  28. Hirel B, Le Gouis J, Ney B, Gallais A (2007) The challenge of improving nitrogen use efficiency in crop plants: towards a more central role for genetic variability and quantitative genetics within integrated approaches. J Exp Bot 58:2369–2387

  29. Jiang SS, Liang XN, Li X, Wang SL, Lv DW, Ma CY, Li XH, Ma WJ, Yan YM (2012) Wheat drought-responsive grain proteome analysis by linear and nonlinear 2-DE and MALDI-TOF mass spectrometry. Int J MolSci 13:16065–16083

  30. Kant S, Bi YM, Rothstein SJ (2011) Understanding plant response to nitrogen limitation for the improvement of crop nitrogen use efficiency. J Exp Bot 62:1499–1509

  31. Kichey T, Hirel B, Heumez E, Dubois F, Le Gouis J (2007) In winter wheat (Triticum aestivum L.), post-anthesis nitrogen uptake and remobilisation to the grain correlates with agronomic traits and nitrogen physiological markers. Field Crops Res 102(1):22–32

  32. Kobayashi H, Ikeda TM, Nagata K (2013) Spatial and temporal progress of programmed cell death in the developing starchy endosperm of rice. Planta 237:1393–1400

  33. Kondhare KR, Hedden P, Kettlewell PS, Farrell AD, Monaghan JM (2014) Use of the hormone-biosynthesis inhibitors fluridone and paclobutrazol to determine the effects of altered abscisic acid and gibberellin levels on pre-maturity α-amylase formation in wheat grains. J Cereal Sci 60(1):210–216

  34. Kong L, Wang F, Feng B, Li S, Si J, Zhang B (2010) The structural and photosynthetic characteristics of the exposed peduncle of wheat (Triticum aestivum L.): an important photosynthate source for grain-filling. BMC Plant Biol 10:141

  35. Kong L, Wang F, Si J, Feng B, Zhang B, Li S, Wang Z (2013) Increasing in ROS levels and callose deposition in peduncle vascular bundles of wheat (Triticum aestivum L.) grown under nitrogen deficiency. J Plant Interact 8:109–116

  36. Krugman T, Chagué V, Peleg Z, Balzergue S, Just J, Korol AB, Nevo E, Saranga Y, Chalhoub B, Fahima T (2010) Multilevel regulation and signalling processes associatedwith adaptation to terminal drought in wild emmer wheat. Funct Integr Genomics 10:167–186

  37. Lee S, Seo PJ, Lee HJ, Park CM (2012) A NAC transcription factor NTL4 promotes reactive oxygen species production during drought-induced leaf senescence in Arabidopsis. Plant J 70:831–844

  38. Lur HS, Setter TL (1993) Role of auxin in maize endosperm development. Plant Physiol 103:273–280

  39. Mackintosh C (2004) Dynamic interactions between 14-3-3 proteins and phosphoproteins regulate diverse cellular processes. Biochem J 381:329–342

  40. Martínez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchell RAC, Paul MJ (2011) Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol 156(1):373–381

  41. Meng F, Liu H, Wang K, Liu L, Wang S, Zhao Y, Yin J, Li Y (2013) Development-associated microRNAs in grains of wheat (Triticum aestivum L.). BMC Plant Biol 13:140

  42. Neer EJ, Schmidt CJ, Nambudripad R, Smith TF (1994) The ancient regulatory protein family of WD-repeat proteins. Nature 371:297–300

  43. Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11–35

  44. Nohzadeh Malakshah S, Habibi Rezaei M, Heidari M, Salekdeh GH (2007) Proteomics reveals new salt responsive proteins associated with rice plasma membrane. Biosci Biotechnol Biochem 71:2144–2154

  45. Noodén LD, Guiamét JJ, John I (1997) Senescence mechanisms. Physiol Plant 101:746–753

  46. O’Hara LE, Paul MJ, Wingler A (2013) How do sugars regulate plant growth and development? New insight into the role of trehalose-6-phosphate. Mol Plant 6:261–274

  47. Rasmussen RD, Hole D, Hess JR, Carman JG (1997) Wheat kernel dormancy and +abscisic acid level following exposure to fluridone. J Plant Physiol 150:440–445

  48. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP (2002) MicroRNAs in plants. Gene Dev 16:1616–1626

  49. Rijavec T, Kovac M, Kladnik A, Chourey PS, Dermastia MA (2009) Comparative study on the role of cytokinins in caryopsis development in the maize miniature1 seed mutant and its wild type. J Integr Plant Biol 51:840–849

  50. Roberts MR (2003) 14-3-3 Proteins find new partners in plant cell signalling. Trends Plant Sci 8:218–223

  51. Roberts IN, Caputo C, Kade M, Criado MV, Barneix AJ (2011) Subtilisin-like serine proteases involved in N remobilization during grain filling in wheat. Acta Physiol Plant 33:1997–2001

  52. Ruan YL, Jin Y, Yang YJ, Li GJ, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3:942–955

  53. Schoonheim PJ, Sinnige MP, Casaretto JA, Veiga H, Bunney TD, Quatrano RS, de Boer AH (2007) 14-3-3 adaptor proteins are intermediates in ABA signal transduction during barley seed germination. Plant J 49:289–301

  54. Seiler C, Harshavardhan VT, Rajesh K, Reddy PS, Strickert M, Rolletschek H, Scholz U, Wobus U, Sreenivasulu N (2011) ABA biosynthesis and degradation contributing to ABA homeostasis during barley seed development under control and terminal drought-stress conditions. J Exp Bot 62:2615–2632

  55. Semenov MA, Halford NG (2009) Identifying target traits and molecular mechanisms for wheat breeding under a changing climate. J Exp Bot 60:2791–2804

  56. Sha A, Chen Y, Ba H, Shan Z, Zhang X, Wu X, Qiu D, Chen S, Zhou X (2012) Identification of Glycine Max MicroRNAs in response to phosphorus deficiency. J Plant Biol 55(4):268–280

  57. Slimane RB, Bancal P, Bancal MO (2013) Down-regulation by stems and sheaths of grain filling with mobilized nitrogen in wheat. Field Crops Res 140:59–68

  58. Smith TF, Gaitatzes C, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185

  59. Song J, Jiang L, Jameson PE (2012) Co-ordinate regulation of cytokinin gene family members during flag leaf and reproductive development in wheat. BMC Plant Biol 12:78

  60. Sreenivasulu N, Radchuk V, Strickert M, Miersch O, Weschke W, Wobus U (2006) Gene expression patterns reveal tissue-specific signaling networks controlling programmed cell death and ABA- regulated maturation in developing barley seeds. Plant J 47(2):310–327

  61. Stamova BS, Laudencia-Chingcuanco D, Beckles DM (2009) Transcriptomic analysis of starch biosynthesis in the developing grain of hexaploid wheat. Int J Plant Genomics. Article ID 407426

  62. Sunkar R, Zhou X, Zheng Y, Zhang W, Zhu JK (2008) Identification of novel and candidate miRNAs in rice by high throughput sequencing. BMC Plant Biol 8:25

  63. Suzuki T, Matsuura T, Kawakami N, Noda K (2000) Accumulation and leakage of abscisic acid during embryo development and seed dormancy in wheat. Plant Growth Regul 30:253–260

  64. Tasleem-Tahir A, Nadaud I, Girousse C, Martre P, Marion D, Branlard G (2011) Proteomic analysis of peripheral layers during wheat (Triticum aestivum L.) grain development. Proteomics 11:371–379

  65. Thiel J (2014) Development of endosperm transfer cells in barley. Front Plant Sci 5:108

  66. Tietz A, Ludwig M, Dingkuhn M, Dorffling K (1981) Effect of abscisic acid on the transport of assimilates in barley. Planta 152:557–561

  67. Travaglia C, Cohen AC, Reinoso H, Castillo C, Bottini R (2007) Exogenous abscisic acid increases carbohydrate accumulation and redistribution to the grains in wheat grown under field conditions of soil water restriction. J Plant Growth Regul 26:285–289

  68. Travaglia C, Reinoso H, Cohen A, Luna C, Tommasino E, Castillo C, Bottini R (2010) Exogenous ABA increases yield in field-grown wheat with moderate water restriction. J Plant Growth Regul 29:366–374

  69. Uauy C, Distelfeld A, Fahima T, Blechl A, Dubcovsky J (2006) A NAC gene regulating senescence improves grain protein, Zinc, and Iron content in wheat. Science 314:1298–1301

  70. Wan Y, Shewry PR, Hawkesford MJ (2013) A novel family of γ-gliadin genes are highly regulated by nitrogen supply in developing wheat grain. J Exp Bot 64:161–168

  71. Weichert N, Saalbach I, Weichert H, Kohl S, Erban A, Kopka J, Hause B, Varshney A, Sreenivasulu N, Strickert M, Kumlehn J, Weschke W, Weber H (2010) Increasing sucrose uptake capacity of wheat grains stimulates storage protein synthesis. Plant Physiol 152:698–710

  72. Wingler A, Purdy S, MacLean JA, Pourtau N (2006) The role of sugars in integrating environmental signals during the regulation of leaf senescence. J Exp Bot 57:391–399

  73. Xiong LM, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

  74. Xu FX, Lagudah ES, Moose SP, Riechers DE (2002) Tandemly duplicated safener-induced glutathione S-transferase genes from Triticumtauschii contribute to genome- and organ specific expression in hexaploid wheat. Plant Physiol 130:362–373

  75. Xue LJ, Zhang JJ, Xue HW (2009) Characterization and expression profiles of miRNAs in rice seeds. Nucleic Acids Res 37:916–930

  76. Yadav UP, Ivakov A, Feil R, Duan GY, Walther D, Giavalisco P, Piques M, Carillo P, Hubberten HM, Stitt M, Lunn JE (2014) The sucrose-trehalose 6-phosphate (Tre6P) nexus: specificity and mechanisms of sucrose signalling by Tre6P. J Exp Bot 65(4):1051–1068

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

  78. Yang J, Peng S, Visperas RM, Sanico AL, Zhu Q, Gu S (2000a) Grain filling pattern and cytokinin content in the grains and roots of rice. Plant Growth Regul 30:261–270

  79. Yang J, Zhang J, Huang Z, Zhu Q, Wang L (2000b) Remobilization of carbon reserves is improved by controlled soil-drying during grain filling of wheat. Crop Sci 40:1645–1655

  80. Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323

  81. Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2002) Abscisic acid and cytokinins in the root exudates and leaves and their relations with senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling. Planta 215:645–652

  82. Yang J, Zhang J, Wang Z, Zhu Q, Liu L (2003a) Involvement of abscisic acid and cytokinins in the senescence and remobilization of carbon reserves in wheat subjected to water stress during grain filling. Plant Cell Env 26:1621–1631

  83. Yang JC, Zhang JH, Wang ZQ, Zhu QS (2003b) Hormones in the grains in relation to sink strength and postanthesis development of spikelets in rice. Plant Growth Regul 41:185–195

  84. Yang J, Zhang J, Ye Y, Wang Z, Zhu Q, Liu L (2004) Involvement of abscisic acid and ethylene in the responses of rice grains to water stress during filling. Plant Cell Env 27:1055–1064

  85. Yang J, Zhang J, Liu K, Wang Z, Liu L (2006) Abscisic acid and ethylene interact in wheat grains in response to soil drying during grain filling. New Phytol 171:293–303

  86. Yang F, Jørgensen AD, Li H, Søndergaard I, Finnie C, Svensson B, Jiang D, Wollenweber B, Jacobsen S (2011) Implications of high-temperature events and water deficits on protein profiles in wheat (Triticum aestivum L. cv. Vinjett) grain. Proteomics 11:1684–1695

  87. Yin LL, Xue HW (2012) The MADS29 transcription factor regulates the degradation of the nucellus and the nucellar projection during rice seed development. Plant Cell 24:1049–1065

  88. Young TE, Gallie DR (1999) Analysis of programmed cell death in wheat endosperm reveals differences in endosperm development between cereals. Plant Mol Biol 39:915–926

  89. Zhan S, Lukens L (2010) Identification of novel miRNAs and miRNA dependent developmental shifts of gene expression in Arabidopsis thaliana. PLoS One 5(4):e10157

  90. Zhang ZX, Chen J, Lin S, Li Z, Cheng RH, Fang CX, Chen HF, Lin WX (2012) Proteomic and phosphoproteomic determination of ABA’s effects on grain-filling of Oryza sativa L. inferior spikelets. Plant Sci 185:259–273

  91. 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(2):e89140

  92. Zhu QH, Spriggs A, Matthew L, Fan L, Kennedy G, Gubler F, Helliwell CA (2008) A diverse set of microRNAs and microRNA-like small RNAs in developing rice grains. Genome Res 18:1456–1465

  93. 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 62:3907–3916

Download references

Acknowledgments

This work was supported by the Shandong and National Earmarked Fund for Modern Agro-industry Technology Research System (SDAIT-04, CARS-3-1-21) and the Special Fund for Agroscientific Research on Public Causes, MOA of China (201303109-7, 201203079).

Author information

Correspondence to Lingan Kong.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kong, L., Guo, H. & Sun, M. Signal transduction during wheat grain development. Planta 241, 789–801 (2015). https://doi.org/10.1007/s00425-015-2260-1

Download citation

Keywords

  • Grain development
  • Hormones
  • Senescence
  • Signal transduction
  • Wheat (Triticum aestivum L)