Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Internode elongation pattern, internode diameter and hormone changes in soybean (Glycine max) under different shading conditions

Rui Zhang https://orcid.org/0000-0003-0385-1663 A , Fuxin Shan A , Chang Wang A , Chao Yan A , Shoukun Dong A , Yao Xu https://orcid.org/0000-0002-4963-6881 A , Zhenping Gong A and Chunmei Ma A B
+ Author Affiliations
- Author Affiliations

A Northeast Agricultural University, Changjiang Road No. 600, Harbin, Heilongjiang 150030, P.R. China,

B Corresponding author. Email: chunmm518@163.com

Crop and Pasture Science 71(7) 679-688 https://doi.org/10.1071/CP20071
Submitted: 10 March 2020  Accepted: 9 June 2020   Published: 7 July 2020

Abstract

Internode length and diameter in soybean (Glycine max (L.) Merr.) are closely associated with lodging. The pattern of internode elongation and increase in internode diameter and factors involved were studied in two soybean cultivars, HN48 (tall-stem cultivar) and HN60 (dwarf cultivar), in the growing seasons of 2017 and 2018. Four treatments included natural lighting, shading of the apical meristem, covering of all internodes with aluminium foil, and whole-plant shading with plastic shading nets. When the number of internodes (N) on the main stem was >3, internode N began to elongate. Internode N – 1 exhibited the most rapid elongation, and internode N – 2 elongated slowly. Internode N – 3 stopped elongating, but the increase in internode diameter did not cease as internode elongation stopped. Shading the soybean apical meristem, the stem, and the whole plant all led to internode elongation. Different shading conditions did not alter the pattern of internode elongation. Soybean stem and apical meristem were both light-sensitive tissues. With an increase in shading, internode length increased, whereas internode diameter decreased. Contents of gibberellic acid (GA3) and salicylic acid in the stem also increased, but abscisic acid content decreased. Shading reduced the size of starch grains but increased the number of osmiophilic granules in the chloroplast. Elevated GA3 level was the main cause of the changes in internode length and diameter induced by shading. These results suggest that reduction in GA3 synthesis and enhancement in carbohydrates formation could a strategy for soybean plants to avoid lodging.

Additional keywords: ABA, chloroplast ultrastructure, increased internode diameter.


References

Anderson JM (1982) The role of chlorophyll-protein complexes in the function and structure of chloroplast thylakoids. Molecular and Cellular Biochemistry 46, 161–172.
The role of chlorophyll-protein complexes in the function and structure of chloroplast thylakoids.Crossref | GoogleScholarGoogle Scholar | 6750355PubMed |

Baldev B, Lang A, Agatep AO (1965) Gibberellin production in pea seeds developing in excised pods: effect of growth retardant AMO-1618. Science 147, 155–157.
Gibberellin production in pea seeds developing in excised pods: effect of growth retardant AMO-1618.Crossref | GoogleScholarGoogle Scholar | 14220443PubMed |

Ballaré CL, Scopel AL, Sánchez RA (1990) Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies. Science 247, 329–332.
Far-red radiation reflected from adjacent leaves: an early signal of competition in plant canopies.Crossref | GoogleScholarGoogle Scholar | 17735851PubMed |

Barendse GWM, Lang A (1972) Comparison of endogenous gibberellins and of the fate of applied radioactive gibberellin A1 in a normal and a dwarf strain of Japanese morning glory. Plant Physiology 49, 836–841.
Comparison of endogenous gibberellins and of the fate of applied radioactive gibberellin A1 in a normal and a dwarf strain of Japanese morning glory.Crossref | GoogleScholarGoogle Scholar |

Bensen RJ, Beall FD, Mullet JE, Morgan PW (1990) Detection of endogenous gibberellins and their relationship to hypocotyl elongation in soybean seedlings. Plant Physiology 94, 77–84.
Detection of endogenous gibberellins and their relationship to hypocotyl elongation in soybean seedlings.Crossref | GoogleScholarGoogle Scholar | 16667722PubMed |

Bown AW, Crozier RA (1975) The effect of light on the gibberellin metabolism and growth of Phaseolus coccineus seedlings. Planta 126, 83–91.
The effect of light on the gibberellin metabolism and growth of Phaseolus coccineus seedlings.Crossref | GoogleScholarGoogle Scholar | 24430090PubMed |

Chrispeels MJ, Varner JE (1966) Inhibition of gibberellic acid induced formation of α-amylase by abscisin II. Nature 212, 1066–1067.
Inhibition of gibberellic acid induced formation of α-amylase by abscisin II.Crossref | GoogleScholarGoogle Scholar |

Cosgrove DJ, Sovonick-Dunford SA (1989) Mechanism of gibberellin-dependent stem elongation in peas. Plant Physiology 89, 184–191.
Mechanism of gibberellin-dependent stem elongation in peas.Crossref | GoogleScholarGoogle Scholar | 11537446PubMed |

Dayan J, Voronin N, Gong F, Sun T, Hedden P, Fromm H, Aloni R (2012) Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems. The Plant Cell 24, 66–79.
Leaf-induced gibberellin signaling is essential for internode elongation, cambial activity, and fiber differentiation in tobacco stems.Crossref | GoogleScholarGoogle Scholar | 22253226PubMed |

Fan Y, Chen J, Cheng Y, Raza MA, Wu X, Wang Z, Liu Q, Wang R, Wang X, Yong T, Liu W, Liu J, Du J, Shu K, Yang W, Yang F (2018) Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize–soybean relay-strip intercropping system. PLoS One 13, e0198159
Effect of shading and light recovery on the growth, leaf structure, and photosynthetic performance of soybean in a maize–soybean relay-strip intercropping system.Crossref | GoogleScholarGoogle Scholar | 30379963PubMed |

Feng L, Raza MA, Li Z, Chen Y, Khalid MHB, Du J, Liu W, Wu X, Song C, Yu L, Zhang Z, Yuan S, Yang W, Yang F (2019) The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean. Frontiers in Plant Science 9, 1952
The influence of light intensity and leaf movement on photosynthesis characteristics and carbon balance of soybean.Crossref | GoogleScholarGoogle Scholar | 30687355PubMed |

Franklin KA, Whitelam GC (2005) Phytochromes and shade-avoidance responses in plants. Annals of Botany 96, 169
Phytochromes and shade-avoidance responses in plants.Crossref | GoogleScholarGoogle Scholar | 15894550PubMed |

Garrison R (1973) The growth and development of internodes in Helianthus. Botanical Gazette 134, 246–255.
The growth and development of internodes in Helianthus.Crossref | GoogleScholarGoogle Scholar |

Garrison R, Briggs WR (1972) Internodal growth in localized darkness. Botanical Gazette 133, 270–276.
Internodal growth in localized darkness.Crossref | GoogleScholarGoogle Scholar |

Gawronska H, Yang YY, Furukawa K, Kendrick RE, Takahashi N, Kamiya Y (1995) Effects of low irradiance stress on gibberellin levels in pea seedlings. Plant & Cell Physiology 36, 1361–1367.
Effects of low irradiance stress on gibberellin levels in pea seedlings.Crossref | GoogleScholarGoogle Scholar |

Gommers CMM, Visser EJW, St Onge KR, Voesenek LACJ, Pierik R (2013) Shade tolerance: when growing tall is not an option. Trends in Plant Science 18, 65–71.
Shade tolerance: when growing tall is not an option.Crossref | GoogleScholarGoogle Scholar |

Hussain S, Iqbal N, Pang T, Khan MN, Liu W-G, Yang W-Y (2019a) Weak stem under shade reveals the lignin reduction behavior. Journal of Integrative Agriculture 18, 496–505.
Weak stem under shade reveals the lignin reduction behavior.Crossref | GoogleScholarGoogle Scholar |

Hussain S, Iqbal N, Rahman T, Liu T, Brestic M, Safdar MH, Asghar MA, Farooq MU, Shafiq I, Ali A, Shoaib M, Chen G, Qin S, Liu W, Yang W (2019b) Shade effect on carbohydrates dynamics and stem strength of soybean genotypes. Environmental and Experimental Botany 162, 374–382.
Shade effect on carbohydrates dynamics and stem strength of soybean genotypes.Crossref | GoogleScholarGoogle Scholar |

Hussain S, Iqbal N, Brestic M, Raza MA, Pang T, Langham DR, Safdar ME, Ahmed S, Wen B, Gao Y, Liu W, Yang W (2019c) Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment. The Science of the Total Environment 658, 626–637.
Changes in morphology, chlorophyll fluorescence performance and Rubisco activity of soybean in response to foliar application of ionic titanium under normal light and shade environment.Crossref | GoogleScholarGoogle Scholar | 30580217PubMed |

Hussain S, Liu T, Iqbal N, Brestic M, Pang T, Mumtaz M, Shafiq I, Li S, Wang L, Gao Y, Khan A, Ahmad I, Allakhverdiev SI, Liu W, Yang W (2020a) Effects of lignin, cellulose, hemicellulose, sucrose and monosaccharide carbohydrates on soybean physical stem strength and yield in intercropping. Photochemical & Photobiological Sciences 19, 462–472.
Effects of lignin, cellulose, hemicellulose, sucrose and monosaccharide carbohydrates on soybean physical stem strength and yield in intercropping.Crossref | GoogleScholarGoogle Scholar |

Hussain S, Pang T, Iqbal N, Shafiq I, Skalicky M, Brestic M, Safdar ME, Mumtaz M, Ahmad A, Asghar MA, Raza A, Allakhverdiev SI, Wang Y, Wang XC, Yang F, Yong T, Liu W, Yang W (2020b) Acclimation strategy and plasticity of different soybean genotypes in intercropping. Functional Plant Biology 47, 592–610.
Acclimation strategy and plasticity of different soybean genotypes in intercropping.Crossref | GoogleScholarGoogle Scholar | 32375994PubMed |

Islam MA, Tarkowská D, Clarke JL, Blystad DR, Gislerød HR, Torre S, Olsen JE (2014) Impact of end-of-day red and far-red light on plant morphology and hormone physiology of poinsettia. Scientia Horticulturae 174, 77–86.
Impact of end-of-day red and far-red light on plant morphology and hormone physiology of poinsettia.Crossref | GoogleScholarGoogle Scholar |

Jing Z, Smith DL, Weiguo L, Xinfu C, Wenyu Y (2011) Effects of shade and drought stress on soybean hormones and yield of main-stem and branch. African Journal of Biotechnology 10, 14392–14398.
Effects of shade and drought stress on soybean hormones and yield of main-stem and branch.Crossref | GoogleScholarGoogle Scholar |

Kigel J (1980) The role of the leaves in the regulation of internode elongation in Phaseolus vulgaris. Physiologia Plantarum 49, 161–168.
The role of the leaves in the regulation of internode elongation in Phaseolus vulgaris.Crossref | GoogleScholarGoogle Scholar |

Kucera B, Cohn MA, Leubnermetzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.
Plant hormone interactions during seed dormancy release and germination.Crossref | GoogleScholarGoogle Scholar |

Kumudini S, Singh G (2010) Soybean growth and development. In ‘The soybean: botany, production and uses’. pp. 48–73. (CAB International: Wallingford, UK) 10.1079/9781845936440.0048

Kurepin LV, Pharis RP (2014) Light signaling and the phytohormonal regulation of shoot growth. Plant Science 229, 280–289.
Light signaling and the phytohormonal regulation of shoot growth.Crossref | GoogleScholarGoogle Scholar | 25443853PubMed |

Kurepin LV, Emery RJN, Pharis RP, Reid DM (2007) Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: putative roles for plant hormones in leaf and internode growth. Journal of Experimental Botany 58, 2145–2157.
Uncoupling light quality from light irradiance effects in Helianthus annuus shoots: putative roles for plant hormones in leaf and internode growth.Crossref | GoogleScholarGoogle Scholar | 17490995PubMed |

Kurepin LV, Walton LJ, Hayward A, Neil Emery RJ, Reid DM, Chinnappa CC (2012) Shade light interaction with salicylic acid in regulating growth of sun (alpine) and shade (prairie) ecotypes of Stellaria longipes. Plant Growth Regulation 68, 1–8.
Shade light interaction with salicylic acid in regulating growth of sun (alpine) and shade (prairie) ecotypes of Stellaria longipes.Crossref | GoogleScholarGoogle Scholar |

Liu W, Zou J, Zhang J, Yang F, Wan Y, Yang W (2015) Evaluation of soybean (Glycine max) stem vining in maize–soybean relay strip intercropping system. Proceedings of the Japan Academy 91, 69–75.
Evaluation of soybean (Glycine max) stem vining in maize–soybean relay strip intercropping system.Crossref | GoogleScholarGoogle Scholar |

Liu W, Deng Y, Hussain S, Zou J, Yuan J, Luo L, Yang C, Yuan X, Yang W (2016) Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean [Glycine max (L.) Merr.]. Field Crops Research 196, 261–267.
Relationship between cellulose accumulation and lodging resistance in the stem of relay intercropped soybean [Glycine max (L.) Merr.].Crossref | GoogleScholarGoogle Scholar |

Liu X, Rahman T, Song C, Su B, Yang F, Yong T, Wu Y, Zhang C, Yang W (2017) Changes in light environment, morphology, growth and yield of soybean in maize–soybean intercropping systems. Field Crops Research 200, 38–46.
Changes in light environment, morphology, growth and yield of soybean in maize–soybean intercropping systems.Crossref | GoogleScholarGoogle Scholar |

Liu W, Hussain S, Ting L, Zou J-L, Ren M-L, Zhou T, Liu J, Yang F, Yang W-Y (2019) Shade stress decreases stem strength of soybean through restraining lignin biosynthesis. Journal of Integrative Agriculture 18, 43–53.
Shade stress decreases stem strength of soybean through restraining lignin biosynthesis.Crossref | GoogleScholarGoogle Scholar |

Morrison TA, Kessler JR, Buxton DR (1994) Maize internode elongation patterns. Crop Science 34, 1055–1060.
Maize internode elongation patterns.Crossref | GoogleScholarGoogle Scholar |

Nemoto K, Morita S, Baba T (1995) Shoot and root development in rice related to the phyllochron. Crop Science 35, 24–29.
Shoot and root development in rice related to the phyllochron.Crossref | GoogleScholarGoogle Scholar |

Ren B, Cui H, Camberato JJ, Dong S, Liu P, Zhao B, Zhang J (2016) Effects of shading on the photosynthetic characteristics and mesophyll cell ultrastructure of summer maize. Naturwissenschaften 103, 67
Effects of shading on the photosynthetic characteristics and mesophyll cell ultrastructure of summer maize.Crossref | GoogleScholarGoogle Scholar | 27437706PubMed |

Shao Q, Wang H, Guo H, Zhou A, Huang Y, Sun Y, Li M (2014) Effects of shade treatments on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii. PLoS One 9, e85996
Effects of shade treatments on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii.Crossref | GoogleScholarGoogle Scholar | 25165817PubMed |

Stitt M, Zeeman SC (2012) Starch turnover: pathways, regulation and role in growth. Current Opinion in Plant Biology 15, 282–292.
Starch turnover: pathways, regulation and role in growth.Crossref | GoogleScholarGoogle Scholar | 22541711PubMed |

Travaglia C, Reinoso H, Bottini R (2009) Application of abscisic acid promotes yield in field-cultured soybean by enhancing production of carbohydrates and their allocation in seed. Crop & Pasture Science 60, 1131
Application of abscisic acid promotes yield in field-cultured soybean by enhancing production of carbohydrates and their allocation in seed.Crossref | GoogleScholarGoogle Scholar |

Umezaki T (1998) Internode elongation characteristics of indeterminate type plants of soybean. Japanese Journal of Crop Science 67, 187–192.
Internode elongation characteristics of indeterminate type plants of soybean.Crossref | GoogleScholarGoogle Scholar | [in Japanese with English Abstract]

Vicente D, Schuster I, Lazzari F, Paranzini JPD, de Oliveira MAR, Prete CEC (2016) Mapping and validation of molecular markers of genes Dt1 and Dt2 to determine the type of stem growth in soybean. Acta Scientiarum Agronomy 38, 61

Wu Y, Gong W, Yang W (2017) Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean. Scientific Reports 7, 9259
Shade inhibits leaf size by controlling cell proliferation and enlargement in soybean.Crossref | GoogleScholarGoogle Scholar | 28835715PubMed |

Yang F, Fan Y, Wu X, Cheng Y, Liu Q, Feng L, Chen J, Wang Z, Wang X, Yong T, Liu W, Liu J, Du J, Shu K, Yang W (2018) Auxin-to-gibberellin ratio as a signal for light intensity and quality in regulating soybean growth and matter partitioning. Frontiers in Plant Science 9, 56–71.
Auxin-to-gibberellin ratio as a signal for light intensity and quality in regulating soybean growth and matter partitioning.Crossref | GoogleScholarGoogle Scholar | 29441084PubMed |

Yuan Y, Yang WY (2007) Effects of shading on endogenous hormone of Cardiocrinum giganteum. Northern Horticulture 123–125. [in Chinese with English Abstract]

Zivcak M, Brestic M, Kalaji HM, Govindjee (2014) Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light? Photosynthesis Research 119, 339–354.
Photosynthetic responses of sun- and shade-grown barley leaves to high light: is the lower PSII connectivity in shade leaves associated with protection against excess of light?Crossref | GoogleScholarGoogle Scholar | 24445618PubMed |