Advances in understanding the graft healing mechanism: a review of factors and regulatory pathways

Abstract

Grafting is a widely used technique for asexual plant reproduction, especially in agriculture and forestry. This procedure is used to shorten the seedling period, improve the structure of scion branches, and help plants adapt to difficult environments. Although grafting has numerous benefits, several obstacles remain to be overcome. The connection between scion and rootstock is regulated by various factors, including phytohormones and molecular mechanisms, which are crucial for graft healing. This review provides an overview of recent advances in the field of grafting, with a specific focus on the factors and regulatory pathways that influence graft healing. The ultimate goal is to aid understanding of how to achieve successful grafting between plants and create desirable grafting chimeras. We provide an overview of the latest developments in plant grafting, covering aspects related to morphology, physiology, and molecular biology. We also discuss research directions in polyploid breeding and long-distance transfer of small molecules in grafted plants.

Acknowledgements

I thank all members of the State Key Laboratory for Efficient Production of Forest Resources for useful discussions. This work was supported by the National Natural Science Foundation of China (No. 32371857 and No. 32071793), the Special Foundation for National Science and Technology Basic Research Program of China (No. 2019FY100803), and the innovation and application of new Sapindus species for soap and efficient breeding technology (No. 2023 N3005).

Author contributions

L.W., Y.L., J.L., and T.Z. conceived the study. L.W. and Y.L. wrote the manuscript. J.L., T.Z., and Z.C. revised the manuscript. L.J. and Z.C. supervised the work.

Data availability statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article.

Conflict of interest statement

The authors have no competing interests.

References

[1] He W, Xie R, Luo L. et al. Comparative transcriptomic analysis of inarching invigorating rootstock onto incompatible grafts in citrus. Int J Mol Sci. 2022; 23:14523

[2] Liu BH, Cheng L, Zhang JX. et al. Evaluation of five rootstocks on the growth, gas exchanges and chlorophyll fluorescence of Juglans regia L. cv. ’Xiangling’. Hortic Sci. 2023; 50:208-18

[3] Jordana CN, Stapleton SC, Colee JC. et al.How does watermelon grafting impact fruit yield and quality? A systematic review. HortScience. 2023; 58:836-45

[4] Shonerd RH, Thompson AA, Wortman SE. Effects of rootstock and location on open field ‘BHN 589’ and ‘Nebraska wedding’ grafted tomato yield. HortScience. 2023; 11:1393-9

[5] Zhang W, Thieme CJ, Kollwig G. et al. tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell. 2016; 28:1237-49

[6] Mauro RP, Stazi SR, Distefano M. et al. Yield and compositional profile of eggplant fruits as affected by phosphorus supply, genotype and grafting. Horticulturae. 2022; 8:304

[7] Liu X, Li J, Huang M. et al. Mechanisms for the influence of citrus rootstocks on fruit size. J Agric Food Chem. 2015; 63:2618-27

[8] Alejandro S, Höller S, Meie B. et al. Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci. 2020; 11:1-23

[9] Mauro RP, Agnello M, Onofri A. et al. Scion and rootstock differently influence growth, yield and quality characteristics of cherry tomato. Plan Theory. 2020; 9:1725

[10] Warschefsky EJ, Klein LL, Frank MH. et al. Rootstocks: diversity, domestication, and impacts on shoot phenotypes. Trends Plant Sci. 2015; 21:418-37

[11] Tedesco S, Fevereiro P, Kragler F. et al. Plant grafting and graft incompatibility: a review from the grapevine perspective. Sci Hortic. 2022; 299:111019

[12] Muhammed MAA, Mohamed AKSH, Qayyum MF. et al. Physiological response of mango transplants to phytohormones under salinity stress. Sci Hortic. 2022; 296:110918

[13] Luan H, Niu C, Nie X. et al. Transcriptome and physiological analysis of rootstock types and silicon affecting cold tolerance of cucumber seedlings. Plan Theory. 2022; 11:445

[14] Morales-Olmedo MG, Sellés G, Pinto M. et al. Full-field characterization of sweet cherry rootstocks: responses to soil with different air-filled porosities. Plant Soil. 2021;1-17

[15] Thomas H, Van den Broeck L, Spurney R. et al. Gene regulatory networks for compatible versus incompatible grafts identify a role for SlWOX4 during junction formation. Plant Cell. 2022; 34:535-56

[16] Thomas HR, Gevorgyan A, Frank MH. Anatomical and biophysical basis for graft incompatibility within the Solanaceae. J Exp Bot. 2023; 74:4461-70

[17] Goldschmidt EE. Plant grafting: new mechanisms, evolutionary implications. Front Plant Sci. 2014; 5:727

[18] Notaguchi M, Kurotani KI, Sato Y. et al. Cell-cell adhesion in plant grafting is facilitated by β-1,4-glucanases. Science. 2020; 369:698-702

[19] Wulf KE, Reid JB, Foo E. What drives interspecies graft union success? Exploring the role of phylogenetic relatedness and stem anatomy. Physiol Plant. 2020; 170:132-47

[20] He W, Xie R, Wang Y. et al. Comparative transcriptomic analysis on compatible/incompatible grafts in citrus. Hortic Res. 2022;9:uhab072

[21] Rasool A, Mansoor S, Bhat KM, et al. Mechanisms underlying graft union formation and rootstock scion interaction in horticultural plants. Front Plant Sci. 2020; 11:590847.

[22] Mostakhdemi A, Sadeghi-Majd R, Najafabad MZB. et al. Evaluation of patch budding success in Persian walnut affected by different treatments after budding. Int J Fruit Sci. 2022; 22:495-503

[23] Chowdhury BDB, Son Y-J, Kubota C. et al. Automated workflow analysis in vegetable grafting using an ultra-wide band based real-time indoor location tracking system. Comput Electron Agric. 2022; 194:106773

[24] Vanderstraeten L, Sanchez-Muñoz R, Depaepe T. et al. Mix-and-match: an improved, fast and accessible protocol for hypocotyl micrografting of Arabidopsis seedlings with systemic ACC responses as a case study. Plant Methods. 2022; 18:24

[25] Ebadi A, Solgi M, Zamani Z. Effects of date of grafting and kind of callusing bed on grafting success of side and saddle grafting in Persian walnut (Juglans regia L.). Seed Plant. 2002; 18:294-305

[26] Ahmed N, Singh SR, Srivastava KK. et al. Effect of different environments, grafting methods, and times on sprouting, graft success and plant growth of walnut (Juglans regia). Indian J Agric Sci. 2012; 82:1022-6

[27] Ruseani NS, Vanhove W, Susilo AW. et al. Clonal differences in nitrogen use efficiency and macro-nutrient uptake in young clonal cocoa (Theobroma cacao L.. seedlings from Indonesia. J Plant Nutr. 2022; 45:3196-211

[28] Sedaghathoor S, Noie M. Study on different grafting methods of kiwifruit ‘Hayward’ on the ‘Matua’ and ‘Bruno’ rootstocks. Fruits. 2016; 71:275-80

[29] Nisar N, Verma S, Pogson BJ. et al. Inflorescence stem grafting made easy in Arabidopsis. Plant Methods. 2012; 8:50

[30] Bartusch K, Melnyk CW. Insights into plant surgery: an overview of the multiple grafting techniques for Arabidopsis thaliana. Front Plant Sci. 2020; 11:613442

[31] Feng M, Zhang A, Nguyen V. et al. A conserved graft formation process in Norway spruce and Arabidopsis identifies the PAT gene family as central regulators of wound healing. Nat Plants. 2024; 10:53-65

[32] Tsutsui H, Kawakatsu Y, Notaguchi M. Micrografting in Arabidopsis using a silicone Chip. Bio Protoc. 2021; 11:e4053

[33] Li Z, Ma F, Zhang H. et al. Grafting techniques of Tung tree seedlings with Hypocotyle rootstocks and the anatomical structure. Scientia Silvae Sinicae. 2024; 60:80-92

[34] Loupit G, Brocard L, Ollat N. et al. Grafting in plants: recent discoveries and new applications. J Exp Bot. 2023; 74:2433-47

[35] Yin H, Yan B, Sun J. et al. Graft-union development: a delicate process that involves cell-cell communication between scion and stock for local auxin accumulation. J Exp Bot. 2012; 63:4219-32

[36] Devi P, DeVetter L, Kraft M. et al. Micrographic view of graft union formation between watermelon Scion and squash rootstock. Front. Plant Sci. 2022; 13:878289

[37] Yıldırım PM, Dolgun O. et al. Graft formation in some spur and vigorous apple varieties grafted on Ottawa 3 rootstock: a histological investigation. J Food Agric Environ. 2010; 8:512-4

[38] Li D, Han F, Liu X. et al. Localized graft incompatibility in kiwifruit: analysis of homografts and heterografts with different rootstock & scion combinations. Sci Hortic. 2021; 283:0304-4238

[39] Cheong YH, Chang H-S, Gupta R. et al. Transcriptional profiling reveals novel interactions between wounding, pathogen, abiotic stress, and hormonal responses in Arabidopsis. Plant Physiol. 2002; 129:661-77

[40] Mittler R, Zandalinas SI, Fichman Y. et al. Reactive oxygen species signalling in plant stress responses. Nat Rev Mol Cell Biol. 2022; 23:663-79

[41] Hander T, Fernandez-Fernan Á, Kumpf RP. et al. Damage on plants activates Ca2+- dependent metacaspases for release of immunomodulatory peptides. Science. 2019;363:eaar7486

[42] Sözen C, Schenk ST, Boudsocq M. et al. Wounding and insect feeding trigger two independent MAPK pathways with distinct regulation and kinetics. Plant Cell. 2020; 32:1988-2003

[43] Danquah A, Zelicourt AD, Colcombet J. et al. The role of ABA and MAPK signaling pathways in plant abiotic stress responses. Biotechnol Adv. 2014; 32:40-52

[44] Daher FB, Chen Y, Bozorg B. et al. Anisotropic growth is achieved through the additive mechanical effect of material anisotropy and elastic asymmetry. elife. 2018; 7:e38161

[45] Howe GA, Major IT, Koo AJ. Modularity in jasmonate signaling for multistress resilience. Annu Rev Plant Biol. 2018; 69:387-415

[46] Zhang Y, Turner JG. Wound-induced endogenous jasmonates stunt plant growth by inhibiting mitosis. PLoS One. 2008; 3:e3699

[47] Basu D, Haswell ES. Plant mechanosensitive ion channels: an ocean of possibilities. Curr Opin Plant Biol. 2017; 40:43-8

[48] Mielke S, Zimmer M, Meena MK. et al. Jasmonate biosynthesis arising from altered cell walls is prompted by turgor-driven mechanical compression. Sci Adv. 2021;7:eabf0356

[49] Zhang G, Zhao F, Chen L. et al. Jasmonate-mediated wound signalling promotes plant regeneration. Nat Plants. 2019; 5:491-7

[50] Souza CA, Li S, Lin AZ. et al. Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol. 2017; 173:2383-98

[51] Hoermayer L, Montesinos JC, Marhava P. et al.Wounding-induced changes in cellular pressure and localized auxin signalling spatially coordinate restorative divisions in roots. Proc Natl Acad Sci USA. 2020; 117:15322-31

[52] Jonsson K, Kierzkowski D. et al. Lathe RS, Mechanochemical feedback mediates tissue bending required for seedling emergence. Curr Biol. 2021; 31:1154-1164.e3

[53] Matsuoka K, Sato R, Matsukura Y. et al. Wound-inducible ANAC071 and ANAC096 transcription factors promote cambial cell formation in incised Arabidopsis flowering stems. Commun Biol. 2021; 4:369

[54] Rahimi A, Karami O, Lestari AD. et al. Control of cambium initiation and activity in Arabidopsis by the transcriptional regulator AHL15. Curr Biol. 2022; 32:1764-1775.e3

[55] Sachs T. Integrating cellular and organismic aspects of vascular differentiation. Plant Cell Physiol. 2000; 41:649-56

[56] Nanda AK, Melnyk CW. The role of plant hormones during grafting. J Plant Res. 2018; 131:49-58

[57] Melnyk CW, Schuster C, Leyser O. et al. Developmental framework for graft formation and vascular reconnection in Arabidopsis thaliana. Curr Biol. 2015; 25:1306-18

[58] Melnyk CW, Gabel A, Hardcastle TJ. et al. Transcriptome dynamics at Arabidopsis graft junctions reveal an intertissue recognition mechanism that activates vascular regeneration. Proc Natl Acad Sci USA. 2018;115:E2447-56

[59] Mazur E, Benková E, Friml J. et al. Vascular cambium regeneration and vessel formation in wounded inflorescence stems of Arabidopsis. Sci Rep. 2016; 6:33754

[60] Pitaksaringkarn W, Matsuoka K, Asahina M. et al. XTH20 and XTH19 regulated by ANAC071 under auxin flow are involved in cell proliferation in incised Arabidopsis inflorescence stems. Plant J. 2014; 80:604-14

[61] Fisher K, Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol. 2007; 17:1061-6

[62] Hirakawa Y, Shinohara H, Kondo Y. et al. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci USA. 2008; 105:15208-13

[63] Ikeuchi M, Iwase A, Ito T. et al. Wound-inducible WUSCHEL-RELATED HOMEOBOX 13 is required for callus growth and organ reconnection. Plant Physiol. 2022; 188:425-41

[64] Suer S, Agusti J, Sanchez P. et al. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011; 23:3247-3259.15

[65] Iwase A, Mitsuda N, Koyama T. et al. The AP2/ERF transcription factor WIND1 controls cell dedifferentiation in Arabidopsis. Curr Biol. 2011; 21:508-14

[66] Inoue T, Higuchi M, Hashimoto Y. et al. Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature. 2001; 409:1060-3

[67] Mähönen AP, Bonke M, Kauppinen L. et al. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 2000; 14:2938-43

[68] Mason MG, Mathews DE, Argyros DA. et al. Multiple type-B response regulators mediate cytokinin signal transduction in Arabidopsis. Plant Cell. 2005; 17:3007-18

[69] Mo Z, Feng G, Su W. et al. Transcriptomic analysis provides insights into grafting union development in pecan (Carya illinoiensis). Genes. 2018; 9:71

[70] Zhou CM, Li JX, Zhang TQ. et al. The structure of B-ARR reveals the molecular basis of transcriptional activation by cytokinin. Proc Natl Acad Sci USA. 2024; 121:e2319335121

[71] Argyros RD, Mathews DE, Chiang Y-H. et al. Type B response regulators of arabidopsis play key roles in cytokinin signaling and plant development. The Plant Cell. 2008; 20:2102-16

[72] Liu S, Strauss S, Adibi M. et al. Cytokinin promotes growth cessation in the Arabidopsis root. Curr Biol. 2022; 32:1974-1985.e3

[73] Dewitte W, Scofield S, Alcasabas AA. et al. Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokinin responses. Proc Natl Acad Sci USA. 2007; 104:14537-42

[74] Randall RS, Miyashima S, Blomster T. et al. AINTEGUMENTA and the D-type cyclin CYCD3;1 regulate root secondary growth and respond to cytokinins. Biol Open. 2015; 4:1229-36

[75] Hertle AP, Haberl B, Bock R. Horizontal genome transfer by cell-to-cell travel of whole organelles. Sci Adv. 2021;7:eabd8215

[76] Thomas CL, Bayer EM, Ritzenthaler C. et al. Specific targeting of a Plasmodesmal protein affecting cell-to-cell communication. PLoS Biol. 2008; 6:e7

[77] Baluška F, Šamaj J, Napier R. et al. Maize calreticulin localizes preferentially to plasmodesmata in root apex. Plant J. 1999; 19:481-8

[78] Gao YQ, Chen JG, Chen ZR. et al. A new vesicle trafficking regulator CTL1 plays a crucial role in ion homeostasis. PLoS Biol. 2017; 15:e2002978

[79] Kitagawa M, Paultre D, Rademaker H. Intercellular communication via plasmodesmata. New Phytol. 2015; 205:970-2

[80] Pina A, Errea P, Schulz A. et al. Cell-to-cell transport through plasmodesmata in tree callus cultures. Tree Physiol. 2009; 29:809-18

[81] Vatén A, Dettmer J, Wu S. et al. Callose biosynthesis regulates symplastic trafficking during root development. Dev Cell. 2011; 21:1144-55

[82] Nicolas WJ, Grison MS, Trepout S. et al. Architecture and permeability of post-cytokinesis plasmodesmata lacking cytoplasmic sleeves. Nat Plants. 2017; 3:17082

[83] Yan D, Yadav SR, Paterlini A. et al. PLM modulates phloem unloading through sphingolipid biosynthesis and plasmodesmal ultrastructure. Nat Plants. 2019; 5:604-15

[84] Maule AJ, Gaudioso-Pedraza R, Benitez-Alfonso Y. Callose deposition and symplastic connectivity are regulated prior to lateral root emergence. Commun Integr Biol. 2013; 6:e26531

[85] Li ZP, Paterlini A, Glavier M. et al. Intercellular trafficking via plasmodesmata: molecular layers of complexity. Cell Mol Life Sci. 2021; 78:799-816

[86] Stahl Y, Faulkner C. Receptor complex mediated regulation of Symplastic traffic. Trends Plant Sci. 2016; 21:450-9

[87] Wu SW, Kumar R, Iswanto ABB. et al. Callose balancing at plasmodesmata. J Exp Bot. 2018; 69:5325-39

[88] Hunter K, Kimura S, Rokka A. et al. CRK2 enhances salt tolerance by regulating callose deposition in connection with PLD α 1. Plant Physiol. 2019; 180:2004-21

[89] Vu MH, Hyun TK, Bahk S. et al. ROS-mediated plasmodesmal regulation requires a network of an Arabidopsis receptor-like kinase, calmodulin-like proteins, and callose synthases. Front Plant Sci. 2023; 13:1107224

[90] Amsbury S, Kirk P, Benitez-Alfonso Y. Emerging models on the regulation of intercellular transport by plasmodesmata-associated callose. J Exp Bot. 2017; 69:105-15

[91] Sun Y, Huang D, Chen X. Dynamic regulation of plasmodesmatal permeability and its application to horticultural research. Hortic Res. 2019; 6:47

[92] Müller J, Toev T, Heisters M. et al. Iron-dependent callose deposition adjusts root meristem maintenance to phosphate availability. Dev Cell. 2015; 33:216-30

[93] O’Lexy R, Kasai K, Clark N. et al. Exposure to heavy metal stress triggers changes in plasmodesmatal permeability via deposition and breakdown of callose. J Exp Bot. 2018; 69:3715-28

[94] Levy A, Zheng JY, Lazarowitz SG. Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr Biol. 2015; 25:2018-25

[95] Kno K, Wan P, Kriechbaume V. et al. Putting the squeeze on Plasmodesmata: a role for reticulons in primary plasmodesmata formation. Plant Physiol. 2015; 168:1563-72

[96] Kriechbaumer V, Botchway SW, Slade SE. et al. Reticulomics: protein-protein interaction studies with two plasmodesmata-localized reticulon family proteins identify binding partners enriched at plasmodesmata, endoplasmic reticulum, and the plasma membrane. Plant Physiol. 2015; 169:1933-45

[97] Brunkard JO, Xu M, Scarpin MR. et al. TOR dynamically regulates plant cell-cell transport. Proc Natl Acad Sci USA. 2020; 117:5049-58

[98] Kurotani KI, Notaguchi M. Cell-to-cell connection in plant grafting-molecular insights into symplasmic reconstruction. Plant Cell Physiol. 2021; 62:1362-71

[99] Fuentes I, Stegemann S, Golczyk H. et al. Horizontal genome transfer as an asexual path to the formation of new species. Nature. 2014; 511:232

[100] Stegemann S, Greiner S. et al. Keuthe M, Horizontal transfer of chloroplast genomes between plant species. Proc Natl Acad Sci USA. 2012; 109:2434-8

[101] Flaishman MA, Loginovsky K, Golobowich S. et al. Arabidopsis thaliana as a model system for graft union development in homografts and heterografts. J Plant Growth Regul. 2008; 27:231

[102] Miao L, Li Q, Sun TS. et al. Sugars promote graft union development in the heterograft of cucumber onto pumpkin. Hortic Res. 2021; 8:146

[103] Chen Z, Zhao J, Hu F. et al. Transcriptome changes between compatible and incompatible graft combination of Litchi chinensis by digital gene expression profile. Sci Rep. 2017; 7:3954

[104] Matsuoka K, Sugawara E, Aoki R. et al. Differential cellular control by cotyledon-derived phytohormones involved in graft reunion of Arabidopsis hypocotyls. Plant Cell Physiol. 2016; 57:2620-31

[105] Guo Y, Qin G, Hongya G. et al. Dof5.6/HCA2, a Dof transcription factor gene, regulates Interfascicular cambium formation and vascular tissue development in Arabidopsis. Plant Cell. 2009; 21:3518-34

[106] Zhang Z, Zheng Y, Ham B-K. et al. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat Plants. 2016; 2:16033

[107] Smit ME, McGregor SR, Sun H. et al. A PXY-mediated transcriptional network integrates signaling mechanisms to control vascular development in Arabidopsis. Plant Cell. 2020; 32:319-35

[108] Fàbregas N, Formosa-Jordan P, Confraria A. et al. Auxin influx carriers control vascular patterning and xylem differentiation in Arabidopsis thaliana. PLoS Genet. 2015; 11:e1005183

[109] Xu T, Dai N, Chen J. et al. Cell surface ABP1-TMK auxin-sensing complex activates ROP GTPase signaling. Science. 2014; 343:1025-8

[110] Kepinski S, Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 2005; 435:446-51

[111] Benjamins R, Scheres B. Auxin: the looping star in plant development. Annu Rev Plant Biol. 2008; 59:443-65

[112] Smetana O, Mäkilä R, Lyu M. et al. High levels of auxin signalling define the stem-cell organizer of the vascular cambium. Nature. 2019; 565:485-9

[113] Bishopp A, Help H, El-Showk S. et al. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol. 2011; 21:917-26

[114] Brackmann K, Qi J, Gebert M. et al. Spatial specificity of auxin responses coordinates wood formation. Nat Commun. 2018; 9:875

[115] Ursache R, Miyashima S, Chen Q. et al. Tryptophan-dependent auxin biosynthesis is required for HD-ZIP III-mediated xylem patterning. Development. 2014; 141:1250-9

[116] Marsch-Martínez N, Franken J, Gonzalez-Aguilera KL. et al. An efficient flat-surface collar-free grafting method for Arabidopsis thaliana seedlings. Plant Methods. 2013; 9:14

[117] Tasheva K, Kosturkova G. The effect of sucrose concentration on in vitro callogenesis of golden root - endangered medicinal plant. Sci Bull F Biotechnol. 2014; 18:77-82

[118] Dellero Y, Berardocco S, Bouchereau A. U-13C-glucose incorporation into source leaves of Brassica napus highlights light-dependent regulations of metabolic fluxes within central carbon metabolism. J Plant Physiol. 2024; 292:154162

[119] Moreno MJC, Hevin C, Ollat N. et al. Developments at the graft interface in homo- and hetero-grafts: gene expression and histological changes during the first month after grafting. Plant Signal Behav. 2014; 9:e28852

[120] Zhang Y, Fu X, Feng Y. et al. Abscisic acid mediates salicylic acid induced chilling tolerance of grafted cucumber by activating H2O2 biosynthesis and accumulation. Int J Mol Sci. 2022; 23:16057

[121] Amano R, Nakayama H, Momoi R. et al. Molecular basis for natural vegetative propagation via regeneration in north American lake cress, Rorippa aquatica (Brassi-caceae). Plant Cell Physiol. 2020; 61:353-69

[122] Wang J, Li D, Chen N. et al. Plant grafting relieves asymmetry of jasmonic acid response induced by wounding between scion and rootstock in tomato hypocotyl. PLoS One. 2020; 15:e0241317

[123] Tanaka H, Hashimoto N, Kawai S. et al. Auxin-induced WUSCHEL-RELATED HOMEOBOX13 mediates asymmetric activity of callus formation upon cutting. Plant Cell Physiol. 2023; 64:305-16

[124] Coşkun ÖF. The effect of grafting on morphological, physiological and molecular changes induced by drought stress in cucumber. Sustain For. 2023; 15:875

[125] Jiao S, Zeng F, Huang Y. et al. Physiological, biochemical and molecular responses associated with drought tolerance in grafted grapevine. BMC Plant Biol. 2023; 23:110

[126] Wu X, Yuan D, Bian X. et al. Transcriptome analysis showed that tomato-rootstock enhanced salt tolerance of grafted seedlings was accompanied by multiple metabolic processes and gene differences. Front. Plant Sci. 2023; 14:1167145

[127] Zhang A, Matsuoka K, Kareem A. et al. Cell-wall damage activates DOF transcription factors to promote wound healing and tissue regeneration in Arabidopsis thaliana. Curr Biol. 2022; 32:1883-1894.e7

[128] Yang L, Xia L, Zeng Y. et al. Grafting enhances plants drought resistance: current understanding, mechanisms, and future perspectives. Front. Plant Sci. 2022; 13:1015317

[129] Feng M, Augstein F, Kareem A. et al. Plant grafting: molecular mechanisms and applications. Mol Plant. 2024; 17:75-91

[130] Tomkins M, Hoerbst F, Gupta S. et al. Exact Bayesian inference for the detection of graft-mobile transcripts from sequencing data. J R Soc Interface. 2022; 19:20220644

[131] Liu Z, Yu X, Qin A. et al. Research strategies for single-cell transcriptome analysis in plant leaves. Plant J. 2022; 112:27-37

[132] Hao L, Zhang Y, Wang S. et al. A constitutive and drought-responsive mRNA undergoes long-distance transport in pear (Pyrus betulaefolia) phloem. Plant Sci. 2020; 293:110419

[133] Cho SK, Sharma P, Butler NM. et al. Polypyrimidine tract-binding proteins of potato mediate tuberization through an interaction with StBEL5 RNA. J Exp Bot. 2015; 66:6835-47

[134] Yang L, Perrera V, Saplaoura E. et al. m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr Biol. 2019; 29:2465-76

[135] Ham BK, Lucas WJ. Phloem-mobile RNAs as systemic signaling agents. Annu Rev Plant Biol. 2016; 68:173

[136] Wang S, Duan X, Wang S. et al. A chaperonin containing T-complex polypeptide-1 facilitates the formation of the PbWoxT1-PbPTB3 ribonucleoprotein complex for long-distance RNA trafficking in Pyrus betulaefolia. New Phytol. 2023; 238:1115-28

[137] Tsaballa A, Xanthopoulou A, Madesis P. et al. Vegetable grafting from a molecular point of view: the involvement of epigenetics in rootstock-Scion interactions. Front. Plant Sci. 2021; 11:621999

[138] Kundariya H, Yang X, Morton K. et al. MSH1-induced heritable enhanced growth vigor through grafting is associated with the RdDM pathway in plants. Nat Commun. 2020; 11:5343

[139] Kapazoglou A, Tani E, Avramidou EV. et al. Epigenetic changes and transcriptional reprogramming upon Woody Plant grafting for crop sustainability in a changing environment. Front. Plant Sci. 2021; 11:613004

[140] Tonosaki K, Fujimoto R, Dennis ES. et al. Will epigenetics be a key player in crop breeding? Front. Plant Sci. 2022; 13:958350

[141] Stegemann S, Bock R. Exchange of genetic material between cells in plant tissue grafts. Science. 2009; 324:649-51

[142] Thyssen G, Svab Z, Maliga P. Cell-to-cell movement of plastids in plants. Proc Natl Acad Sci USA. 2012; 109:2439-43

[143] Li Y, Liang J, Deng B. et al. Applications and prospects of CRISPR/Cas9-Mediated Base editing in plant breeding. Curr Issues Mol Biol. 2023; 45:918-35

[144] Timofejeva L, Singh D. Editorial: methods and applications of CRISPR technology in plant sciences. Front Plant Sci. 2023; 14:1207257

[145] Yang L, Machin F, Wang S. et al. Heritable transgene-free genome editing in plants by grafting of wild-type shoots to transgenic donor rootstocks. Nat Biotechnol. 2023; 41:958-67

[146] Reeves G, Tripathi A, Singh P. et al. Monocotyledonous plants graft at the embryonic root-shoot interface. Nature. 2022; 602:280-6