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Effects of Mycorrhizal Symbiosis on Growth Behavior and Carbohydrate Metabolism of Trifoliate Orange Under Different Substrate P Levels

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Abstract

The carbohydrate regulatory function of arbuscular mycorrhizal fungi (AMF), associated changes in root morphology, and substrate P level are important in the efficiency of AMF. A pot experiment was carried out to study the effects of AMF (Funneliformis mosseae) on growth response, root morphology, and sucrose metabolism of trifoliate orange [Poncirus trifoliata (L.) Raf.] seedlings under varying P substrate levels (0, 3, and 30 mM). Mycorrhizal inoculation stimulated growth performance, biomass production (root and shoot fresh weight), and various root morphological traits, regardless of substrate P level. AMF-induced sucrose accumulation in leaves was more highly positively correlated with leaf sucrose synthase (synthesis direction) activity in AMF than in non-AMF seedlings. Root glucose and fructose concentrations were significantly increased by AMF inoculation, independent of P level. Root colonization was more highly correlated with root glucose than with root fructose. AMF inoculation represented varied effects on activity of acid invertase and neutral invertase in leaves and roots at all the three P levels. These results indicated that AMF-accelerated better growth response and root morphological traits were independent of substrate P level, and AMF-induced sucrose cleavage was dependent on substrate P levels, plant tissue types, and sucrose-cleaving enzyme types.

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References

  • Amor Y, Haigler CH, Jonhson S, Wainscott M, Delmer DP (1995) A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 92:9353–9357

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bago B, Preffer PE, Abubaker J, Jun J, Allen JW, Brouillette J, Douds DD, Lammers PJ, Shachar-Hill Y (2003) Carbon export from arbuscular mycorrhizal roots involves the translocation of carbohydrate as well as lipid. Plant Physiol 131:1496–1507

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baier MC, Keck M, Godde V, Niehaus K, Kuster H, Hohnjec N (2010) Knockdown of the symbiotic sucrose synthase MtSucS1 affects arbuscule maturation and maintenance in mycorrhizal roots of Medicago truncatula. Plant Physiol 152:1000–1014

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Beltrano J, Rusitti M, Agrango MC, Ronco M (2013) Effects of arbuscular mycorrhiza inoculation on plant growth, biological and physiological parameters and mineral nutrition in pepper grown under different salinity and p levels. J Soil Sci Plant Nutr 13:123–141

    Google Scholar 

  • Berta G, Fusconi A, Trotta A (1993) VA mycorrhizal infection and the morphology and function of root systems. Environ Exp Bot 33:159–173

    Article  Google Scholar 

  • Blee KA, Anderson AJ (2002) Transcripts for genes encoding soluble acid invertase and sucrose synthase accumulate in root tip and cortical cells containing mycorrhizal arbuscules. Plant Mol Biol 50:197–211

    Article  CAS  PubMed  Google Scholar 

  • Braunberger PG, Miller MH, Peterson RL (1991) Effect of phosphorus nutrition on morphological characteristics of vesicular-arbuscular mycorrhizal colonization of maize. New Phytol 119:107–113

    Article  CAS  Google Scholar 

  • Doidy J, van Tuinen D, Lamotte O, Corneillat M, Alcaraz G, Wipf D (2012) The Medicago truncatula sucrose transporter family: characterization and implication of key members in carbon partitioning towards arbuscular mycorrhizal fungi. Mol Plant 5:1346–1358

    Article  CAS  PubMed  Google Scholar 

  • Ferrol N, Pérez-Tienda J (2009) Coordinated nutrient exchange in arbuscular mycorrhiza. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas-functional processes and ecological impact. Springer, Berlin, pp 73–87

    Chapter  Google Scholar 

  • Gohoonia TS, Nielsen NE (2004) Root traits as tools for creating phosphorus efficient crop varieties. Plant Soil 260:47–57

    Article  Google Scholar 

  • Grace EJ, Smith FA, Smith SE (2009) Deciphering the arbuscular mycorrhizal pathway of P uptake in non-responsive plant species. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas-functional processes and ecological impact. Springer, Berlin, pp 89–106

    Chapter  Google Scholar 

  • Grimoldi AA, Kavanova M, Lattanzi FA, Schnyder H (2005) Phosphorus nutrition-mediated effects of arbuscular mycorrhiza on leaf morphology and carbon allocation in perennial ryegrass. New Phytol 168:435–444

    Article  CAS  PubMed  Google Scholar 

  • Guo YP, Chen PZ, Zhang LC, Zhang SL (2003) Phosphorus deficiency stress aggravate photoinhibition of photosynthesis and function of xanthophyll cycle in citrus leaves. Plant Nutr Fertil Sci 9:359–363 (in Chinese with English abstract)

    Google Scholar 

  • Gutjahr C, Casieri L, Paszkowski U (2009) Glomus intraradices induces changes in root system architecture of rice independently of common symbiosis signaling. New Phytol 182:829–837

    Article  PubMed  Google Scholar 

  • Jifon JL, Graham JH, Drouillard DL, Syvertsen JP (2002) Growth depression of mycorrhizal Citrus seedlings grown at high phosphorus supply is mitigated by elevated CO2. New Phytol 153:133–142

    Article  Google Scholar 

  • Li ZX, Xu CZ, Li KP, Yan S, Qu X, Zhang JR (2012) Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone. BMC Plant Biol 12:89

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • López-Bucio J, Hernández-Abreu E, Sánchez-Calderón L, Nieto-Jacobo MF, Simpson J, Herrera-Estrella L (2002) Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol 129:244–256

    Article  PubMed Central  PubMed  Google Scholar 

  • Moscatello S, Famiani F, Projetti S, Farinelli D, Battistelli A (2011) Sucrose synthase dominates carbohydrate metabolism and relative growth rate in growing kiwifruit (Actinidia deliciosa, cv Hayward). Sci Hortic 128:197–205

    Article  CAS  Google Scholar 

  • Ning JC, Cumming JR (2001) Arbuscular mycorrhizal fungi alter phosphorus relations of broomsedge (Andropogon virginicus L.) plants. J Exp Bot 52:1883–1891

    Article  CAS  PubMed  Google Scholar 

  • Padilla IMG, Encina CL (2005) Changes in root morphology accompanying mycorrhizal alleviation of phosphorus deficiency in micropropagated Annona cherimola Mill. plants. Sci Hortic 106:360–369

    Article  CAS  Google Scholar 

  • Peng SB, Eissenstat DM, Graham JH, Williams K, Hodge NC (1993) Growth depression in mycorrhizal citrus at high-phosphorus supply. Plant Physiol 101:1063–1071

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Myc Soc 55:158–161

    Article  Google Scholar 

  • Schaeffer C, Wallenda T, Güttenberger M, Hampp R (1995) Acid invertase mycorrhizal and non-mycorrhizal roots of Norway spruce (Picea abies [L.] Kar) seedlings. New Phytol 129:417–424

    Article  CAS  Google Scholar 

  • Schmidt B, Mononkos M, Sumalan R, Biro B (2010) Suppression of arbuscular mycorrhiza’s development by high concentrations of phosphorus at Tagetes patula L. Res J Agric Sci 42:156–162

    Google Scholar 

  • Schubert A, Allara P, Morte A (2003) Cleavage of sucrose in roots of soybean (Glycine max) colonized by an arbuscular mycorrhizal fungus. New Phytol 161:495–501

    Article  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic Press, New York

    Google Scholar 

  • Srivastava AK, Singh S, Marathe RA (2002) Organic citrus: soil fertility and plant nutrition. J Sustain Agric 19:5–29

    Article  Google Scholar 

  • Trindade AV, Siqueira JO, Sturmer SL (2006) Arbuscular mycorrhizal fungi in papaya plantations of Espírito Santo and Bahia, Brazil. Braz J Microbiol 37:283–289

    Article  Google Scholar 

  • Verma A, Agarwal AK, Dubey RS, Solomon S, Singh SB (2013) Sugar partitioning in sprouting lateral bud and shoot development of sugarcane. Plant Physiol Biochem 62:111–115

    Article  CAS  PubMed  Google Scholar 

  • Wright DP, Read DJ, Scholes JD (1998) Mycorrhizal sink strength influences whole plant carbon balance of Trifolium repens L. Plant, Cell Environ 21:881–891

    Article  Google Scholar 

  • Wu QS, Wang YS, Xia RX (2006) Comparison of arbuscular mycorrhizal fungi for drought resistance of trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Acta Hortic Sin 33:613–616 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Wu QS, Zou YN, He XH, Luo P (2011) Arbuscular mycorrhizal fungi can alter some root characters and physiological status in trifoliate orange (Poncirus trifoliata L. Raf.) seedlings. Plant Growth Regul 65:273–278

    Article  CAS  Google Scholar 

  • Wu QS, He XH, Zou YN, Liu CY, Xiao J, Li Y (2012) Arbuscular mycorrhizas alter root system architecture of Citrus tangerine through regulating metabolism of endogenous polyamines. Plant Growth Regul 68:27–35

    Article  CAS  Google Scholar 

  • Wu QS, Zou YN, Huang YM, Li Y, He XH (2013) Arbuscular mycorrhizal fungi induce sucrose cleavage for carbon supply of arbuscular mycorrhizas in citrus genotypes. Sci Hortic 160:320–325

    Article  CAS  Google Scholar 

  • Zhang ZL, Zai L (2004) Experimental manual of plant physiology, 3rd edn. Higer Education Press, Beijing (in Chinese)

    Google Scholar 

  • Zhang DJ, Xia RX, Cao X, Shu B, Chen CL (2013) Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Sci Hortic 160:389–397

    Article  CAS  Google Scholar 

  • Zobel RW, Alloush GA, Belesky DP (2006) Differential root morphology response to no versus high phosphorus, in three hydroponically grown forage chicory cultivars. Environ Exp Bot 57:201–208

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This study was supported by the Key Project of Chinese Ministry of Education (211107) and the Open Fund of Institute of Root Biology, Yangtze University (R201401).

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Authors and Affiliations

  1. College of Horticulture and Gardening/Institute of Root Biology, Yangtze University, Jingzhou, 434025, Hubei, China

    Qiang-Sheng Wu & Yan Li

  2. National Research Centre for Citrus, Amravati Road, Nagpur, 440 033, Maharashtra, India

    A. K. Srivastava

Authors
  1. Qiang-Sheng Wu
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  2. A. K. Srivastava
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  3. Yan Li
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Correspondence to Qiang-Sheng Wu.

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Wu, QS., Srivastava, A.K. & Li, Y. Effects of Mycorrhizal Symbiosis on Growth Behavior and Carbohydrate Metabolism of Trifoliate Orange Under Different Substrate P Levels. J Plant Growth Regul 34, 499–508 (2015). https://doi.org/10.1007/s00344-015-9485-x

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  • DOI: https://doi.org/10.1007/s00344-015-9485-x

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