Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Roles played by invertase and gene expression in the development of the horn-shaped gall on leaves of Rhus chinensis

Zhen-Yuan Ruan A B C , Xiao-Ming Chen A B D , Pu Yang A B and Bing-Yi Wang A B
+ Author Affiliations
- Author Affiliations

A The Research Institute of Resource Insects, Chinese Academy of Forestry, Bailong Si, Bailong Road, Panlong District, Kunming, China.

B Key Laboratory of Cultivation and Utilisation of Resource Insects of State Forestry Administration, Bailong Si, Bailong Road, Panlong District, Kunming, China.

C Department of Landscape Architecture, Yunnan Forestry Technological College, Jindian 1, Chuanjin Road, Panlong District, Kunming, China.

D Corresponding author. Email: cafcxm@139.com

Functional Plant Biology 44(12) 1160-1170 https://doi.org/10.1071/FP16436
Submitted: 16 December 2016  Accepted: 17 July 2017   Published: 15 August 2017

Abstract

The present study deals with the growth and development of the horn-shaped gall, which is induced by Schlechtendalia chinensis Bell. on leaves of Rhus chinensis Mill. The relationship between gall formers and their host plants was investigated by means of the activities of various invertases, the expressions of the cell wall invertase gene (INV2), and vacuolar invertase gene (INV3) during gall development. Our results show that the increase in the sink strength of the galls required cell wall invertase and vacuolar invertase, and that vacuolar invertase had a particular impact during the early development. In addition, vacuolar invertase activity was always significantly higher in galls than in leaves. However, ionically bound cell wall invertase showed a slightly significant increased activity level when compared with the leaves after galls had entered the fast growing period. This result indicates that vacuolar invertase is related to the rapid expansion of the galls, but ionically bound cell wall invertase is involved in the rapid growth of tissues. The enhanced activity of cell wall invertase and the expression of INV2 may be a plant response to a gall-induced stress. Cytoplasmic invertase that acts as a maintenance enzyme, or takes part in the production of secondary metabolites, was elevated when intracellular acid invertase activity decreased.

Additional keywords: organ expansion, plant–insect relationship, rapid growth of tissue, secondary metabolites, sink strength, stress response.


References

Aksenova NP, Konstantinova TN, Golyanovskaya SA, Sergeeva LI, Romanov GA (2012) Hormonal regulation of tuber formation in potato plants. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 59, 451–466.
Hormonal regulation of tuber formation in potato plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xos1Cru7w%3D&md5=4db7eaed47c044fc26c5efbb18b1ca01CAS |

Bagatto G, Paquette LC, Shorthouse JD (1996) Influence of galls of Phanacis taraxaci on carbon partitioning within common dandelion, Taraxacum officinale. Entomologia Experimentalis et Applicata 79, 111–117.
Influence of galls of Phanacis taraxaci on carbon partitioning within common dandelion, Taraxacum officinale.Crossref | GoogleScholarGoogle Scholar |

Bauerfeind MA, Winkelmann T, Franken P, Druege U (2015) Transcriptome, carbohydrate, and phytohormone analysis of Petunia hybrid reveals a complex disturbance of plant functional integrity under mild chilling stress. Frontiers in Plant Science 6, 583
Transcriptome, carbohydrate, and phytohormone analysis of Petunia hybrid reveals a complex disturbance of plant functional integrity under mild chilling stress.Crossref | GoogleScholarGoogle Scholar |

Burstein M, Wool D, Eshel A (1994) Sink strength and clone size of sympatric, gall-forming aphids. European Journal of Entomology 91, 57–71.

Carlson SJ, Chourey PS (1999) A re-evaluation of the relative roles of two invertases INCW2 and IVR1 in developing maize kernels and other tissues. Plant Physiology 121, 1025–1035.
A re-evaluation of the relative roles of two invertases INCW2 and IVR1 in developing maize kernels and other tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXns12nurw%3D&md5=439cfaf1f54f3954547421940f85a54cCAS |

Castrillon-Arbelaez PA, Delano-Frier JP (2011) The sweet side of inhibition: invertase inhibitors and their importance in plant development and stress responses. Current Enzyme Inhibition 7, 169–177.
The sweet side of inhibition: invertase inhibitors and their importance in plant development and stress responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1yktrzK&md5=7a0672898361d67274c12ee7b90e62f7CAS |

Castro AC, Oliveira DC, Moreira ASFP, Lemas-Filho JP, Isaias RMS (2012) Source–sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae). South African Journal of Botany 83, 121–126.
Source–sink relationship and photosynthesis in the horn-shaped gall and its host plant Copaifera langsdorffii Desf. (Fabaceae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCgtrjO&md5=f0c21b61c5bf8a73eeb5da3688b162fdCAS |

Cho JI, Lee SK, Ko S, Kim HK, Jun SH, Less YH, Bhoo SH, Lee KW, An G, Hahn TR, Jeon JS (2005) Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.). Plant Cell Reports 24, 225–236.
Molecular cloning and expression analysis of the cell-wall invertase gene family in rice (Oryza sativa L.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlt1Wmtbk%3D&md5=dd8d3ac194f5e11fc0706621483b6c35CAS |

De Storme N, Geelen D (2014) The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms. Plant, Cell & Environment 37, 1–18.
The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVyjurbL&md5=8b3456d74798d7b1de71fe52ab6044a7CAS |

Diamond SE, Blair CP, Abrahamson WG (2008) Test the nutrition hypothesis for the adaptive nature of insect galls: does a non-adapted herbivore perform better in galls? Ecological Entomology 33, 385–393.
Test the nutrition hypothesis for the adaptive nature of insect galls: does a non-adapted herbivore perform better in galls?Crossref | GoogleScholarGoogle Scholar |

Eschrich W, Eschrich B (1987) Control of phloem unloading by source activities and light. Plant Physiology and Biochemistry 25, 625–634.

Fahrendorf T, Beck E (1990) Cytosolic and cell-wall-bound acid invertases from leaves of Urtica dioica L.: a comparison. Planta 180, 237–244.
Cytosolic and cell-wall-bound acid invertases from leaves of Urtica dioica L.: a comparison.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXpsFGrtg%3D%3D&md5=2c56eded92c7c943a30dbb2ad30741a1CAS |

Farci D, Collu G, Kirkpatrick J, Esposito F, Piano D (2016) RhVI1 is a membrane-anchored vacuolar invertase highly expressed in Rosa hybrida L. petals. Journal of Experimental Botany 67, 3303–3312.
RhVI1 is a membrane-anchored vacuolar invertase highly expressed in Rosa hybrida L. petals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFSrsbzL&md5=1956049f71d88203582484e02caeebedCAS |

Fotopoulos V, Gilbert M, Pittman J, Marvier AC, Buchana A, Sauer N (2003) The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atßfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum. Plant Physiology 132, 821–829.
The monosaccharide transporter gene, AtSTP4, and the cell-wall invertase, Atßfruct1, are induced in Arabidopsis during infection with the fungal biotroph Erysiphe cichoracearum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslert7Y%3D&md5=adeb7b9d762af8dcdb530db7dc17f790CAS |

Gagné S, Cluzet S, Mérillon JM, Gény L (2011) ABA initiates anthocyanin production in grape cell cultures. Journal of Plant Growth Regulation 30, 1–10.
ABA initiates anthocyanin production in grape cell cultures.Crossref | GoogleScholarGoogle Scholar |

Godt DE, Roitsch T (1997) Regulation and tissue-specific distribution of mRNA for three extracellular invertase isozymes in tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiology 115, 273–282.
Regulation and tissue-specific distribution of mRNA for three extracellular invertase isozymes in tomato suggests an important function in establishing and maintaining sink metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt1ynur0%3D&md5=81fd1ecf714c0e05ee94934ec875eaffCAS |

Haouazine-Takvorian N, Tymowska-Lalanne LZ, Takvorian A, Tregear J, Lejeune B, Lecharmy A, Kreis M (1997) Characterization of two members of Arabidopsis thaliana gene family, Atbfruct3 and Atbfruct4, coding for vacuolar invertase. Gene 197, 239–251.
Characterization of two members of Arabidopsis thaliana gene family, Atbfruct3 and Atbfruct4, coding for vacuolar invertase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXlsFGms7c%3D&md5=661f08087585b9fdebd1481f46ed16d6CAS |

Hayes MA, Davies C, Dry IB (2007) Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential role in sink and source tissues. Journal of Experimental Botany 58, 1985–1997.
Isolation, functional characterization, and expression analysis of grapevine (Vitis vinifera L.) hexose transporters: differential role in sink and source tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFeksLc%3D&md5=0267efc50c8c0bae2a4bffb9080181afCAS |

Hayes MA, Feechan A, Dry IB (2010) Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiology 153, 211–221.
Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnt1Ggsrc%3D&md5=c374a8fe419bffcb2c541a0d1a7b8bddCAS |

Hori K (1992) Insect secretions and their effect on plant growth, with special reference to hemipterans. In ‘Biology of insect-induced galls’. (Eds JD Shorthouse, O Rohfritsch) pp. 157–170. (Oxford University Press: New York)

Hsiao CC, Fu RH, Sung HY (2002) A novel bound form of plant invertase in rice suspension cells. Botanical Bulletin of Academia Sinica 43, 115–122.

Inbar M, Eshel A, Wool D (1995) Interspecific competition among phloem-feeding insects mediated by induced host–plant sinks. Ecology 76, 1506–1515.
Interspecific competition among phloem-feeding insects mediated by induced host–plant sinks.Crossref | GoogleScholarGoogle Scholar |

Ito M (2005) Effect of gall formation by a cynipid wasp, Andricus symbioticus, on the development of the leaves and shoots of Quercus dentate. Entomological Science 8, 229–234.
Effect of gall formation by a cynipid wasp, Andricus symbioticus, on the development of the leaves and shoots of Quercus dentate.Crossref | GoogleScholarGoogle Scholar |

Jain R, Chandra A, Solomon S (2013) Impact of exogenously applied enzymes effectors on sucrose metabolizing enzymes (SPS, SS and SAI) and sucrose content in sugarcane. Sugar Tech 15, 370–378.
Impact of exogenously applied enzymes effectors on sucrose metabolizing enzymes (SPS, SS and SAI) and sucrose content in sugarcane.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXptlaqtQ%3D%3D&md5=46f55b24d35b8b617ee97850d9a8fa15CAS |

Kato K, Hijii N (1997) Effects of gall formation by Dryocosmus kuriphilus Yasumatsu (Hym., Cynipidae) on the growth of chestnut trees. Journal of Applied Entomology 121, 9–15.
Effects of gall formation by Dryocosmus kuriphilus Yasumatsu (Hym., Cynipidae) on the growth of chestnut trees.Crossref | GoogleScholarGoogle Scholar |

Kim JY, Mahé A, Guy S, Brangeon J, Roche O, Chourey PS, Prioul JL (2000a) Characterization of two members of the maize gene family, Incw3 and Incw4, coding cell-wall invertases. Gene 245, 89–102.
Characterization of two members of the maize gene family, Incw3 and Incw4, coding cell-wall invertases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsFamsr4%3D&md5=031da784f17e9a1f986a2c30507a0195CAS |

Kim J-Y, Mahé M, Brangeon J, Prioul J-L (2000b) A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression. Plant Physiology 124, 71–84.
A maize vacuolar invertase, IVR2, is induced by water stress. Organ/tissue specificity and diurnal modulation of expression.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmvVGhtro%3D&md5=2b67e36d6479c692acdaac366a48d304CAS |

Kingston-Smith AH, Walker RP, Pollock CJ (1999) Invertase in leaves: conundrum or control points? Journal of Experimental Botany 50, 735–743.

Koyama Y, Yao I, Akimoto SI (2004) Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation. Entomologia Experimentalis et Applicata 113, 35–44.
Aphid galls accumulate high concentrations of amino acids: a support for the nutrition hypothesis for gall formation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVenurzO&md5=db3e16f34d81f68b8541347bc10edbffCAS |

Leite GHP, Crusciol CAC, De Siqueira GF, Silva MDA, Carpenter SR, Gunderson LH (2015) Plant regulators and invertase activity in sugarcane at the beginning of the harvest season. Ciência Rural 45, 1788–1794.
Plant regulators and invertase activity in sugarcane at the beginning of the harvest season.Crossref | GoogleScholarGoogle Scholar |

Li ZM, Palmer WM, Martin AP, Wang RQ, Rainsford F, Jin Y, Patrick JW, Yang YJ, Ruan YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and tolerance of, young fruit. Journal of Experimental Botany 63, 1155–1166.
High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and tolerance of, young fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Omu7Y%3D&md5=82721ad617888fb40d6935a40537c5bdCAS |

Liu SJ, Lan JX, Zhou BH, Qin YX, Zhou YH, Xiao XH, Yang JH, Gou JQ, Qi JY, Huang YC, Tang CR (2015) HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree). New Phytologist 206, 709–725.
HbNIN2, a cytosolic alkaline/neutral-invertase, is responsible for sucrose catabolism in rubber-producing laticifers of Hevea brasiliensis (para rubber tree).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXkvFCksLc%3D&md5=87f3f4042eed8f4ddefba78b33029a0bCAS |

Llewelyn M (1982) The energy economy of fluid-feeding herbivorous insects. In ‘Insect–plant relationships’. (Eds JH Visser, AK Minks) pp. 243–251. (Center for Agricultural Publishing and Documentation: Wageningen, The Netherlands)

McIntyre PJ, Whitham TG (2003) Plant genotype affects long-term herbivore population dynamics and extinction: conservation implications. Ecology 84, 311–322.
Plant genotype affects long-term herbivore population dynamics and extinction: conservation implications.Crossref | GoogleScholarGoogle Scholar |

Miles PW (1999) Aphid saliva. Biological Reviews of the Cambridge Philosophical Society 74, 41–85.
Aphid saliva.Crossref | GoogleScholarGoogle Scholar |

Miller GL (1959) Use of dinitrosazicylic acid reagent invertase for determination of reducing sugar. Analytical Chemistry 31, 426–428.
Use of dinitrosazicylic acid reagent invertase for determination of reducing sugar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG1MXmtFKiuw%3D%3D&md5=f3e6714eb901c80ce4880a4f5e01e8ccCAS |

Mitsuhashi W, Sasaki S, Kanazawa A, Yang YY, Kamiya Y, Toyomasu T (2004) Differential expression of acid invertase genes during seed germination in Arabidopsis thaliana. Bioscience, Biotechnology, and Biochemistry 68, 602–608.
Differential expression of acid invertase genes during seed germination in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXjt1OktL8%3D&md5=6e9a08c6556f42e508dbb2ccf240360aCAS |

Morris DA, Arthur ED (1986) Stimulation of acid invertase activity by indol-3-yl-acetic acid in tissues undergoing cell expansion. Plant Growth Regulation 4, 259–271.
Stimulation of acid invertase activity by indol-3-yl-acetic acid in tissues undergoing cell expansion.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XkvFCmtLc%3D&md5=86f4e6be945f7dca1660c90cf541b1e5CAS |

Nogal A (2011) Initial stages in the formation of galls induced by Geoica utriacularia in Pistacia terebinthus leaflets: origin of the two vascular bundles which characterize the wall of the galls. American Journal of Plant Sciences 2, 175–179.
Initial stages in the formation of galls induced by Geoica utriacularia in Pistacia terebinthus leaflets: origin of the two vascular bundles which characterize the wall of the galls.Crossref | GoogleScholarGoogle Scholar |

Pan RZ (2001) ‘Plant physiology.’ (Higher Education Press: Beijing)

Patrick JW (1997) Pholem unloading: sieve element unloading and post-sieve element transport. Annual Review of Plant Physiology and Plant Molecular Biology 48, 191–222.
Pholem unloading: sieve element unloading and post-sieve element transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXjs1egu70%3D&md5=94f7a248fbbfeb42ccedc5e336204ad0CAS |

Patrick JW, Botha FC, Birch RG (2013) Metabolic engineering of sugars and simple sugar derivatives in plants. Plant Biotechnology Journal 11, 142–156.
Metabolic engineering of sugars and simple sugar derivatives in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvVOltLs%3D&md5=10a76a00d8f46d1e53e5d520b4640f15CAS |

Pfeiffer I, Kutschera U (1995) Sucrose metabolism and cell elongation in developing sunflower hypocotyls. Journal of Experimental Botany 46, 631–638.
Sucrose metabolism and cell elongation in developing sunflower hypocotyls.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXms1Wltb4%3D&md5=e412da15ff33a9cf72a1ebd6a13090caCAS |

Price PW, Waring GL, Fernandes GW (1986) Hypotheses on the adaptive nature of galls. Proceedings of the Entomological Society of Washington 88, 361–363.

Quick WP, Schaffer AA (1996) Sucrose metabolism in source and sinks. In ‘Photoassimilate distribution in plants and crops: source–sink relationships’. (Eds E Zamski, AA Schaffer) pp. 115–156. (CRC Press: NewYork)

Rabot A, Portemer V, Péron T, Mortreau E, Leduc N, Hamama L, Coutos-Thévenot P, Atanassova R, Sakr S, Gourrierec JL (2014) Interplay of sugar, light and gibberelling in expression of Rosa hybrida vacuolar invertase 1 regulation. Plant & Cell Physiology 55, 1734–1748.
Interplay of sugar, light and gibberelling in expression of Rosa hybrida vacuolar invertase 1 regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xhs1GjurvP&md5=3f7bded3fa08310f2c5c94b7cd33c7e8CAS |

Rausch T, Greiner S (2004) Plant protein inhibitors of invertase. Biochimica et Biophysica Acta. Proteins and Proteomics 1696, 253–261.
Plant protein inhibitors of invertase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVOktLs%3D&md5=73e266c0d1bf5b4b1f2992474f06b4b7CAS |

Rehill BJ, Schultz JC (2003) Enhanced invertase activities in the galls of Hormaphis hamamelidis. Journal of Chemical Ecology 29, 2703–2720.
Enhanced invertase activities in the galls of Hormaphis hamamelidis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVSiu7c%3D&md5=4c68e604f9262b2cbbc1edddb13510bcCAS |

Roa AR, Carcía-Luís A, Barcena JLG, Huguet M (2015) Effect of 2,4-D on fruit sugar accumulation and invertase activity in sweet orange cv. Salustiana. Australian Journal of Crop Science 9, 105–111.

Roitsch T, Sinha AK (2003) Extracellular invertase: key metabolic enzyme and PR protein. Journal of Experimental Botany 54, 513–524.
Extracellular invertase: key metabolic enzyme and PR protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhsFKgtbs%3D&md5=045e42eb2d809ad9a2b6a6161c8552b2CAS |

Roitsch T, Tanner W (1996) Cell wall invertase: bridging the gap. Botanica Acta 109, 90–93.
Cell wall invertase: bridging the gap.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XltVWjsLc%3D&md5=3306fce4cbaf616d7c996239a18c9056CAS |

Rojo E, Zouhar J, Carter C, Kooaleva V, Raikhel NV (2003) A unique mechanism for protein processing and degradation in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 100, 7389–7394.
A unique mechanism for protein processing and degradation in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXkslOmsbo%3D&md5=193e3e4bee8ea2ab39ad143fa252f966CAS |

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. Molecular Plant 3, 942–955.
Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFantLjL&md5=cb52c0eb2ab876c42d2d66bca30bce9aCAS |

Ruan ZY, Chen XM, Yang ZX (2012) Extraction of total RNA from horned-gall and cloning of ACTIN gene fragment. Forest Research 25, 551–557.

Ruan ZY, Chen XM, Yang ZX (2013) Effect of protective enzyme and lipid membrane in Rhus chinensis by the horned-gall formation. Yingyong Kunchong Xuebao 50, 749–757.

Seo SK, Wei A (2008) Probing osmotic effects on invertase with L-(–)-sucrose. Organic & Biomolecular Chemistry 6, 3362–3365.
Probing osmotic effects on invertase with L-(–)-sucrose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFeku7rJ&md5=828da9caf2a0c0858a612b563a846c83CAS |

Sergeeva LI, Keuerntjes JJB, Bentsink L, Vouk J, van der Plas LHW, Koornneef M, Vreugdenhil D (2006) Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proceedings of the National Academy of Sciences of the United States of America 103, 2994–2999.
Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksF2ru7g%3D&md5=aef7b04a39532f277888cef0c0ca8ff1CAS |

Shrestha K, Wilson E, Gay H (2008) Ecological and environmental study of Eupatorium adenophorum Sprengel (Banmara) with reference to its gall formation in Gorkha-Langtang route, Nepal. Journal of Natural History Museum 23, 108–124.

Smeekens S, Rook F (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiology 115, 7–13.
Sugar sensing and sugar-mediated signal transduction in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXmt1ynt7o%3D&md5=21a1eb0de34dc8f2c55f89fc1bd350e5CAS |

Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiology 121, 1–8.
Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtFGls7o%3D&md5=f865c4c7625aea094b2adf8dd6ce82e3CAS |

Sturm A, Chrispeels MJ (1990) cDNA cloning of carrot extracellular β-fructosidase and its expression in response to wounding and bacterial infection. The Plant Cell 2, 1107–1119.

Sturm A, Tang GQ (1999) The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning. Trends in Plant Science 4, 401–407.
The sucrose-cleaving enzymes of plants are crucial for development, growth and carbon partitioning.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2sbgvFWhtQ%3D%3D&md5=81539845fccaefd1692022cca9787fc2CAS |

Suzuki DK, Fukushi Y, Akimoto SI (2009) Do aphid galls provide good nutrients for the aphids?: comparisons of amino acid concentrations in galls among Tetraneura species (Ahididae: Eriosomatinae). Arthropod-Plant Interactions 3, 241–247.
Do aphid galls provide good nutrients for the aphids?: comparisons of amino acid concentrations in galls among Tetraneura species (Ahididae: Eriosomatinae).Crossref | GoogleScholarGoogle Scholar |

Tang GQ, Lüscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sugar partitioning. The Plant Cell 11, 177–189.
Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sugar partitioning.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhsVygtbg%3D&md5=6040887b19dc38604efdcaa02b9f3e15CAS |

Thaker V (1999) Changes in water content, sugars and invertase activity in developing seeds of Hibiscus esculentun. Acta Physiologiae Plantarum 21, 155–159.
Changes in water content, sugars and invertase activity in developing seeds of Hibiscus esculentun.Crossref | GoogleScholarGoogle Scholar |

Tian H, Kong Q, Feng Y, Yu X (2009) Cloning and characterization of a soluble acid invertase-encoding gene from muskmelon. Molecular Biology Reports 36, 611–617.
Cloning and characterization of a soluble acid invertase-encoding gene from muskmelon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhvF2ltLw%3D&md5=33ccaf2154c4ea9212595c38b820b5d9CAS |

Tooker JF, De Moraes CM (2011) Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems. Arthropod-Plant Interactions 5, 115–124.
Feeding by a gall-inducing caterpillar species alters levels of indole-3-acetic and abscisic acid in Solidago altissima (Asteraceae) stems.Crossref | GoogleScholarGoogle Scholar |

Trethewey RN, Geigenberger D, Hennig A, Fleischer-Notter H, Müller-Röber B, Willmitzer L (1999) Induction of the activity of glycolytic enzyme correlates with enhanced hydrolysis of sucrose in the cytosol of transgenic potato tubers. Plant, Cell & Environment 22, 71–79.
Induction of the activity of glycolytic enzyme correlates with enhanced hydrolysis of sucrose in the cytosol of transgenic potato tubers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjs1yisbk%3D&md5=8879c1788be259771b3eff76161d25bfCAS |

Truernit E, Schmid J, Illig J, Sauer N (1996) The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge. The Plant Cell 8, 2169–2182.
The sink-specific and stress-regulated Arabidopsis STP4 gene: enhanced expression of a gene encoding a monosaccharide transporter by wounding, elicitors, and pathogen challenge.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislGhtA%3D%3D&md5=097ba679c80d9e1a9cffe7f1492edb2fCAS |

Vorster DJ, Botha FC (1999) Sugercane intermodal invertases and tissue maturity. Journal of Plant Physiology 155, 470–476.
Sugercane intermodal invertases and tissue maturity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXnslaquro%3D&md5=9344c97aed5d9d5bd1e71e3b3f28af18CAS |

Wang L, Ruan YL (2013) Regulation of cell division and expansion by sugar and auxin signaling. Frontiers in Plant Science 4, 163
Regulation of cell division and expansion by sugar and auxin signaling.Crossref | GoogleScholarGoogle Scholar |

Wang YZ, Zhang DP (2002) Fructose and glucose take part in induction of post-translational inhibitory regulation of acid invertase in apple fruit. Science in China. Series C, Life Sciences 32, 30–39.

Wang J, Wu ZT, Tang XQ (1995) Effects of the horned gall aphid Schlechtendalia chinensis (Bell) on the metabolism of its host Rhus chinensis Mill. Entomological Knowledge 32, 363–366.

Weber H, Borisjuk L, Heim U, Buchner P, Wobus U (1995) Seed coat-associated invertases of fava bean control both unloading and storage functions: cloning of cDNAs and cell type-specific expression. The Plant Cell 7, 1835–1846.

Wool D, Aloni R, Ben-Zvi O, Wollberg M (1999) A galling aphid furnishes its home with a built-in pipeline to the host food supply. Entomologia Experimentalis et Applicata 91, 183–186.
A galling aphid furnishes its home with a built-in pipeline to the host food supply.Crossref | GoogleScholarGoogle Scholar |

Wu LL, Mitchell JP, Cohn NS, Kaufman PB (1993) Gibberellin (GA3) enhances cell wall invertase activity and mRNA levels in elongating dwarf pea (Pisum sativum) shoots. International Journal of Plant Sciences 154, 280–289.
Gibberellin (GA3) enhances cell wall invertase activity and mRNA levels in elongating dwarf pea (Pisum sativum) shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXivFChsb0%3D&md5=f6d4ff9bd45bd0e7162e736487651853CAS |

Xu J, Avigne WT, McCarty DR, Koch KE (1996) A similar dichotomy of sugar modulation and developmental expression affects both paths of sucrose metabolism: evidence from a maize invertase gene family. The Plant Cell 8, 1209–1220.
A similar dichotomy of sugar modulation and developmental expression affects both paths of sucrose metabolism: evidence from a maize invertase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XksFKkurc%3D&md5=e79643718a61a8d4db778fa9120f9615CAS |

Yao Y, Geng MT, Wu XH, Liu J, Li RM, Hu XW, Guo JC (2014) Genome-wide identification, 3D modeling, expression and enzymatic activity analysis of cell wall invertase gene family from Cassava (Manihot esculenta Crantz). International Journal of Molecular Sciences 15, 7313–7331.
Genome-wide identification, 3D modeling, expression and enzymatic activity analysis of cell wall invertase gene family from Cassava (Manihot esculenta Crantz).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXjtFyms78%3D&md5=0feea77b05c778d93f5e45a09d7f0a8bCAS |

Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kuhn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpica R, Zhou YH, Fernie AR (2009) RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiology 150, 1204–1218.
RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXovFertLg%3D&md5=236147e8c580cf8b2a533d95c197040bCAS |

Zhao GF, Liu LX, Hu ZH (1990) Structure and development of the insect-gall of Rhus chinensis. Xibei Zhiwu Xuebao 10, 237–241.

Zhen XM (1998) Different picking period and treatment effect on the contains of gallotannin. Journal of Nanchang University 22, 307–309.