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RESEARCH ARTICLE (Open Access)
Contents Vol 51(6)

Starch and sucrose metabolism plays an important role in the stem development in Medicago sativa

Jierui Wu https://orcid.org/0009-0004-0482-0951 A , Xiaoyu Wang https://orcid.org/0000-0001-7579-1749 A , Lin Bian https://orcid.org/0009-0006-3271-435X A , Zhenyi Li https://orcid.org/0000-0002-6443-484X A , Xiaohong Jiang https://orcid.org/0009-0000-6913-0880 A , Fengling Shi https://orcid.org/0000-0001-7235-1692 A , Fang Tang https://orcid.org/0000-0002-9645-7448 A and Zhiqiang Zhang https://orcid.org/0000-0003-3709-9553 A B *
+ Author Affiliations
- Author Affiliations

A Technology Engineering Center of Drought and Cold-Resistant Grass Breeding in North of the National Forestry and Grassland Administration, College of Grassland, Resources and Environment, Inner Mongolia Agricultural University, Hohhot, China.

B Key Laboratory of Grassland Resources of the Ministry of Education, College of Grassland, Resources and Environment, Inner Mongolia Agricultural University, Hohhot, China.

* Correspondence to: zhangzq1989@imau.edu.cn

Handling Editor: Ravinder Kumar

Functional Plant Biology 51, FP24073 https://doi.org/10.1071/FP24073
Submitted: 18 March 2024  Accepted: 18 April 2024  Published: 13 May 2024

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

The forage quality of alfalfa (Medicago sativa) stems is greater than the leaves. Sucrose hydrolysis provides energy for stem development, with starch being enzymatically converted into sucrose to maintain energy homeostasis. To understand the physiological and molecular networks controlling stem development, morphological characteristics and transcriptome profiles in the stems of two alfalfa cultivars (Zhungeer and WL168) were investigated. Based on transcriptome data, we analysed starch and sugar contents, and enzyme activity related to starch-sugar interconversion. Zhungeer stems were shorter and sturdier than WL168, resulting in significantly higher mechanical strength. Transcriptome analysis showed that starch and sucrose metabolism were significant enriched in the differentially expressed genes of stems development in both cultivars. Genes encoding INV, bglX, HK, TPS and glgC downregulated with the development of stems, while the gene encoding was AMY upregulated. Weighted gene co-expression network analysis revealed that the gene encoding glgC was pivotal in determining the variations in starch and sucrose contents between the two cultivars. Soluble carbohydrate, sucrose, and starch content of WL168 were higher than Zhungeer. Enzyme activities related to sucrose synthesis and hydrolysis (INV, bglX, HK, TPS) showed a downward trend. The change trend of enzyme activity was consistent with gene expression. WL168 stems had higher carbohydrate content than Zhungeer, which accounted for more rapid growth and taller plants. WL168 formed hollow stems were formed during rapid growth, which may be related to the redistribution of carbohydrates in the pith tissue. These results indicated that starch and sucrose metabolism play important roles in the stem development in alfalfa.

Keywords: developmental stage, enzymatic activity, hollow, Medicago sativa L., plant morphology, starch–sugar interconversion, stems, transcriptome.

References

Blaser RE (1964) Symposium on forage utilization: effects of fertility levels and stage of maturity on forage nutritive value. Journal of Animal Science 23(1), 246-253.
| Crossref | Google Scholar |

Boersma M, Gracie AJ, Brown PH (2013) Evidence of mechanical tissue strain in the development of hollow stem in broccoli. Scientia Horticulturae 164, 353-358.
| Crossref | Google Scholar |

Carr SM, Jaffe MJ (1995) Pith autolysis in herbaceous, dicotyledonous plants: experimental manipulation of pith autolysis in several cultivated species. Annals of Botany 75, 587-592.
| Crossref | Google Scholar |

Chang L, Xiao YM, She LF, Xia YP (2013) Analysis of gene expression and enzyme activities related to starch metabolism in Lycoris sprengeri bulbs of different sizes. Scientia Horticulturae 161, 118-124.
| Crossref | Google Scholar |

Cho J-I, Kim H-B, Kim C-Y, Hahn T-R, Jeon J-S (2011) Identification and characterization of the duplicate rice sucrose synthase genes OsSUS5 and OsSUS7 which are associated with the plasma membrane. Molecules and Cells 31, 553-562.
| Crossref | Google Scholar | PubMed |

Doblin MS, Pettolino F, Bacic A (2010) Plant cell walls: the skeleton of the plant world. Functional Plant Biology 37(5), 357-381.
| Crossref | Google Scholar |

Engels FM, Jung HG (1998) Alfalfa stem tissues: cell-wall development and lignification. Annals of Botany 82(5), 561-568.
| Crossref | Google Scholar |

Fils-Lycaon B, Julianus P, Chillet M, Galas C, Hubert O, Rinaldo D, Mbéguié-A-Mbéguié D (2011) Acid invertase as a serious candidate to control the balance sucrose versus (glucose+fructose) of banana fruit during ripening. Scientia Horticulturae 129(2), 197-206.
| Crossref | Google Scholar |

Fugate KK, Eide JD, Martins DN, Grusak MA, Deckard EL, Finger FL (2019) Colocalization of sucrose synthase expression and sucrose storage in the sugarbeet taproot indicates a potential role for sucrose catabolism in sucrose accumulation. Journal of Plant Physiology 240, 153016.
| Crossref | Google Scholar | PubMed |

Gao S, Zhu Y, Zhou L, Fu X, Lei T, Chen Q, et al. (2018) Sucrose signaling function on the formation and swelling of bulblets of Lilium sargentiae E.H. Wilson. Plant Cell, Tissue and Organ Culture (PCTOC) 135, 143-153.
| Crossref | Google Scholar |

Gao M, Zhang S, Luo C, He X, Wei S, Jiang W, et al. (2018b) Transcriptome analysis of starch and sucrose metabolism across bulb development in Sagittaria sagittifolia. Gene 649, 99-112.
| Crossref | Google Scholar | PubMed |

Gill PK, Sharma AD, Singh P, Bhullar SS (2003) Changes in germination, growth and soluble sugar contents of Sorghum bicolor (L.) Moench seeds under various abiotic stresses. Plant Growth Regulation 40, 157-162.
| Crossref | Google Scholar |

Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, et al. (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29(7), 644-652.
| Crossref | Google Scholar | PubMed |

Griffith M, Carling DE (1991) Effects of plant spacing on broccoli yield and hollow stem in Alaska. Canadian Journal of Plant Science 71, 579-585.
| Crossref | Google Scholar |

Hashemi M, Mousavi SM, Razavi SH, Shojaosadati SA (2013) Comparison of submerged and solid state fermentation systems effects on the catalytic activity of Bacillus sp. KR-8104 α-amylase at different pH and temperatures. Industrial Crops and Products 43, 661-667.
| Crossref | Google Scholar |

Huang Q, Xu M, Zhang H, He D, Kong Y, Chen L, Song H (2019) Transcriptome and proteome analyses of the molecular mechanisms associated with coix seed nutritional quality in the process of breeding. Food Chemistry 272, 549-558.
| Crossref | Google Scholar | PubMed |

Jeon J-S, Ryoo N, Hahn T-R, Walia H, Nakamura Y (2010) Starch biosynthesis in cereal endosperm. Plant Physiology and Biochemistry 48(6), 383-392.
| Crossref | Google Scholar | PubMed |

Jung HG, Engels FM (2002) Alfalfa stem tissues: cell wall deposition, composition, and degradability. Crop Science 42(2), 524-534.
| Crossref | Google Scholar |

Kanehisa M, Goto S (2000) KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Research 28(1), 27-30.
| Crossref | Google Scholar | PubMed |

Karley AJ, Ashford DA, Minto LM, Pritchard J, Douglas AE (2005) The significance of gut sucrase activity for osmoregulation in the pea aphid, Acyrthosiphon pisum. Journal of Insect Physiology 51(12), 1313-1319.
| Crossref | Google Scholar | PubMed |

Lamb JFS, Hans-Joachim GJ, Riday H (2012) Harvest impacts on alfalfa stem neutral detergent fiber concentration and digestibility and cell wall concentration and composition. Crop Science 52(5), 2402-2412.
| Crossref | Google Scholar |

LeClere S, Schmelz EA, Chourey PS (2010) Sugar levels regulate tryptophan-dependent auxin biosynthesis in developing maize kernels. Plant Physiology 153(1), 306-318.
| Crossref | Google Scholar | PubMed |

Li S, Liang H, Tao L, Xiong L, Liang W, Shi Z, Zhao Z (2020) Transcriptome sequencing and differential expression analysis reveal molecular mechanisms for starch accumulation in chestnut. Forests 11(4), 388.
| Crossref | Google Scholar |

Li W, Huang D, Wang B, Hou X, Zhang R, Yan M, Liao W (2022) Changes of starch and sucrose content and related gene expression during the growth and development of Lanzhou lily bulb. PLoS ONE 17(1), e0262506.
| Crossref | Google Scholar | PubMed |

Lin Q, Xie Y, Guan W, Duan Y, Wang Z, Sun C (2019) Combined transcriptomic and proteomic analysis of cold stress induced sugar accumulation and heat shock proteins expression during postharvest potato tuber storage. Food Chemistry 297, 124991.
| Crossref | Google Scholar | PubMed |

Liu T, Hu Y, Li X (2008) Comparison of dynamic changes in endogenous hormones and sugars between abnormal and normal Castanea mollissima. Progress in Natural Science 18(6), 685-690.
| Crossref | Google Scholar |

Liu X, Chen L, Shi W, Xu X, Li Z, Liu T, et al. (2021) Comparative transcriptome reveals distinct starch-sugar interconversion patterns in potato genotypes contrasting for cold-induced sweetening capacity. Food Chemistry 334, 127550.
| Crossref | Google Scholar | PubMed |

Martins LF, Kolling D, Camassola M, Dillon AJP, Ramos LP (2008) Comparison of Penicillium echinulatum and Trichoderma reesei cellulases in relation to their activity against various cellulosic substrates. Bioresource Technology 99(5), 1417-1424.
| Crossref | Google Scholar | PubMed |

Mathan J, Singh A, Ranjan A (2021) Sucrose transport and metabolism control carbon partitioning between stem and grain in rice. Journal of Experimental Botany 72(12), 4355-4372.
| Crossref | Google Scholar | PubMed |

Navabi A, Iqbal M, Strenzke K, Spaner D (2006) The relationship between lodging and plant height in a diverse wheat population. Canadian Journal of Plant Science 86(3), 723-726.
| Crossref | Google Scholar |

Neuhaus HE, Emes MJ (2000) Nonphotosynthetic metabolism in plastids. Annual Review of Plant Biology 51(1), 111-140.
| Crossref | Google Scholar |

Pancera SM, Gliemann H, Schimmel T, Petri DFS (2006) Adsorption behavior and activity of hexokinase. Journal of Colloid and Interface Science 302(2), 417-423.
| Crossref | Google Scholar | PubMed |

Paul M (2007) Trehalose 6-phosphate. Current Opinion in Plant Biology 10(3), 303-309.
| Crossref | Google Scholar | PubMed |

Ruan Y-L, Jin Y, Yang Y-J, Li G-J, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Molecular Plant 3(6), 942-955.
| Crossref | Google Scholar | PubMed |

Sheaffer CC, Martin NP, Lamb JFS, Cuomo GR, Jewett JG, Quering SR (2000) Leaf and stem properties of alfalfa entries. Agronomy Journal 92(4), 733-739.
| Crossref | Google Scholar |

Smith AM, Zeeman SC (2020) Starch: a flexible, adaptable carbon store coupled to plant growth. Annual Review of Plant Biology 71, 217-245.
| Crossref | Google Scholar | PubMed |

Wu Y, Sun M, Zhang J, Zhang L, Ren Z, Min R, et al. (2019) Differential effects of paclobutrazol on the bulblet growth of oriental lily cultured in vitro: growth behavior, carbohydrate metabolism, and antioxidant capacity. Journal of Plant Growth Regulation 38, 359-372.
| Crossref | Google Scholar |

Wu J, Wang X, Zhang R, Fu Q, Tang F, Shi F, et al. (2022) Comparative transcriptome and anatomic characteristics of stems in two alfalfa genotypes. Plants 11(19), 2601.
| Crossref | Google Scholar | PubMed |

Xu S-M, Brill E, Llewellyn DJ, Furbank RT, Ruan Y-L (2012) Overexpression of a potato sucrose synthase gene in cotton accelerates leaf expansion, reduces seed abortion, and enhances fiber production. Molecular Plant 5(2), 430-441.
| Crossref | Google Scholar | PubMed |

Yang P, Xu L, Xu H, Tang Y, He G, Cao Y, et al. (2017) Histological and transcriptomic analysis during bulbil formation in Lilium lancifolium. Frontiers in Plant Science 8, 1508.
| Crossref | Google Scholar | PubMed |

Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biology 11(2), R14.
| Crossref | Google Scholar | PubMed |

Zhang L, Lin Q, Feng Y, Fan X, Zou F, Yuan D-Y, Zeng X, Cao H (2015) Transcriptomic identification and expression of starch and sucrose metabolism genes in the seeds of Chinese chestnut (Castanea mollissima). Journal of Agricultural and Food Chemistry 63(3), 929-942.
| Crossref | Google Scholar | PubMed |

Zhang K, Luo K, Li S, Peng D, Tang D, Lu H, et al. (2020) Genetic variation and sequence diversity of starch biosynthesis and sucrose metabolism genes in sweet potato. Agronomy 10(5), 627.
| Crossref | Google Scholar |

Zhao Z, Li R, Wang X, Liang W, Liao J, Huang X, et al. (2022) The starch-sugar interconversion mechanism during bulb development of Cardiocrinum giganteum (Wall.) Makino revealed by transcriptome and metabolite analysis. Industrial Crops and Products 187, 115318.
| Crossref | Google Scholar |

Zhu J, Yu W, Zhang C, Zhu Y, Xu J, Li E, et al. (2020) New insights into amylose and amylopectin biosynthesis in rice endosperm. Carbohydrate Polymers 230, 115656.
| Crossref | Google Scholar | PubMed |