1932

Abstract

Parasitic plants use a special organ, the haustorium, to attach to and penetrate host tissues, forming phloem and/or xylem fusion with the host vascular systems. Across this haustorium–host interface, not only water and nutrients are extracted from the host by the parasitic plant, but also secondary metabolites, messenger RNAs, noncoding RNAs, proteins, and systemic signals are transported between the parasite and host and even among different hosts connected by a parasite. Furthermore, mycorrhizal fungi can form common mycelial networks (CMNs) that simultaneously interconnect multiple plants. Increasing lines of evidence suggest that CMNs can function as conduits, transferring stress-related systemic signals between plants. Between-plant signaling mediated by haustoria and CMNs likely has a profound impact on plant interactions with other organisms and adaptation to environmental factors. Here, we summarize the findings regarding between-plant transfer of biomolecules and systemic signals and the current understanding of the physiological and ecological implications of between-plant signaling.

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2023-05-22
2024-04-24
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Literature Cited

  1. 1.
    Adler LS. 2000. Alkaloid uptake increases fitness in a hemiparasitic plant via reduced herbivory and increased pollination. Amer. Nat. 156:92–99
    [Google Scholar]
  2. 2.
    Alakonya A, Kumar R, Koenig D, Kimura S, Townsley B et al. 2012. Interspecific RNA interference of SHOOT MERISTEMLESS-like disrupts Cuscuta pentagona plant parasitism. Plant Cell 24:3153–66Established a host-induced gene silencing (HIGS) method for studying dodder genes.
    [Google Scholar]
  3. 3.
    Alaux PL, Naveau F, Declerck S, Cranenbrouck S. 2020. Common mycorrhizal network induced JA/ET genes expression in healthy potato plants connected to potato plants infected by Phytophthora infestans. Front. Plant Sci. 11:602
    [Google Scholar]
  4. 4.
    Aly R, Cholakh H, Joel DM, Leibman D, Steinitz B et al. 2009. Gene silencing of mannose 6-phosphate reductase in the parasitic weed Orobanche aegyptiaca through the production of homologous dsRNA sequences in the host plant. Plant Biotechnol. J. 7:487–98
    [Google Scholar]
  5. 5.
    Aly R, Hamamouch N, Abu-Nassar J, Wolf S, Joel DM et al. 2011. Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers. Plant Cell Rep. 30:2233–41
    [Google Scholar]
  6. 6.
    Babikova Z, Gilbert L, Bruce TJ, Birkett M, Caulfield JC et al. 2013. Underground signals carried through common mycelial networks warn neighbouring plants of aphid attack. Ecol. Lett. 16:835–43
    [Google Scholar]
  7. 7.
    Barto EK, Hilker M, Muller F, Mohney BK, Weidenhamer JD, Rillig MC. 2011. The fungal fast lane: Common mycorrhizal networks extend bioactive zones of allelochemicals in soils. PLOS ONE 6:e27195
    [Google Scholar]
  8. 8.
    Bennett AE, Groten K. 2022. The costs and benefits of plant–arbuscular mycorrhizal fungal interactions. Annu. Rev. Plant Biol. 73:649–72
    [Google Scholar]
  9. 9.
    Bennett CW. 1940. Acquisition and transmission of viruses by dodder. Phytopathology 30:649–56
    [Google Scholar]
  10. 10.
    Cai Q, Qiao L, Wang M, He B, Lin FM et al. 2018. Plants send small RNAs in extracellular vesicles to fungal pathogen to silence virulence genes. Science 360:1126–29
    [Google Scholar]
  11. 11.
    Calderwood A, Kopriva S, Morris RJ. 2016. Transcript abundance explains mRNA mobility data in Arabidopsis thaliana. Plant Cell 28:610–15
    [Google Scholar]
  12. 12.
    Cardini A, Pellegrino E, Declerck S, Calonne-Salmon M, Mazzolai B, Ercoli L. 2021. Direct transfer of zinc between plants is channelled by common mycorrhizal network of arbuscular mycorrhizal fungi and evidenced by changes in expression of zinc transporter genes in fungus and plant. Environ. Microbiol. 23:5883–900
    [Google Scholar]
  13. 13.
    Chen WW, Takahashi N, Hirata Y, Ronald J, Porco S et al. 2020. A mobile ELF4 delivers circadian temperature information from shoots to roots. Nat. Plants 6:416–26
    [Google Scholar]
  14. 14.
    Chen X, Yao Q, Gao X, Jiang C, Harberd NP, Fu X. 2016. Shoot-to-root mobile transcription factor HY5 coordinates plant carbon and nitrogen acquisition. Curr. Biol. 26:640–46
    [Google Scholar]
  15. 15.
    Choi WG, Miller G, Wallace I, Harper J, Mittler R, Gilroy S. 2017. Orchestrating rapid long-distance signaling in plants with Ca2+, ROS and electrical signals. Plant J. 90:698–707
    [Google Scholar]
  16. 16.
    Clarke CR, Timko MP, Yoder JI, Axtell MJ, Westwood JH. 2019. Molecular dialog between parasitic plants and their hosts. Annu. Rev. Phytopathol. 57:279–99
    [Google Scholar]
  17. 17.
    Corbesier L, Vincent C, Jang S, Fornara F, Fan Q et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–33
    [Google Scholar]
  18. 18.
    D'Ario M, Griffiths-Jones S, Kim M. 2017. Small RNAs: big impact on plant development. Trends Plant Sci. 22:1056–68
    [Google Scholar]
  19. 19.
    Debock F, Fer A. 1992. Effects of abscisic acid on the transfer of sucrose from host, Pelargonium Zonale (L.) Aiton, to a phanerogamic parasite, Cuscuta reflexa Roxb. Aust. J. Plant Physiol. 19:679–91
    [Google Scholar]
  20. 20.
    Ding C, Zhao Y, Zhang Q, Lin Y, Xue R et al. 2022. Cadmium transfer between maize and soybean plants via common mycorrhizal networks. Ecotoxicol. Environ. Saf. 232:113273
    [Google Scholar]
  21. 21.
    Erb M, Reymond P. 2019. Molecular interactions between plants and insect herbivores. Annu. Rev. Plant Biol. 70:527–57
    [Google Scholar]
  22. 22.
    Fichman Y, Mittler R. 2020. Rapid systemic signaling during abiotic and biotic stresses: Is the ROS wave master of all trades?. Plant J. 102:887–96
    [Google Scholar]
  23. 23.
    Fratianne DG. 1965. The interrelationship between the flowering of dodder and the flowering of some long and short day plants. Amer. J. Bot. 52:556–62
    [Google Scholar]
  24. 24.
    Fu ZQ, Dong X. 2013. Systemic acquired resistance: turning local infection into global defense. Annu. Rev. Plant Biol. 64:839–63
    [Google Scholar]
  25. 25.
    Fujioka H, Samejima H, Suzuki H, Mizutani M, Okamoto M, Sugimoto Y. 2019. Aberrant protein phosphatase 2C leads to abscisic acid insensitivity and high transpiration in parasitic Striga. Nat Plants 5:258–62
    [Google Scholar]
  26. 26.
    Genre A, Lanfranco L, Perotto S, Bonfante P. 2020. Unique and common traits in mycorrhizal symbioses. Nat. Rev. Microbiol. 18:649–60
    [Google Scholar]
  27. 27.
    Green TR, Ryan CA. 1972. Wound-induced proteinase inhibitor in plant leaves: a possible defense mechanism against insects. Science 175:776–77
    [Google Scholar]
  28. 28.
    Halkier BA, Gershenzon J. 2006. Biology and biochemistry of glucosinolates. Annu. Rev. Plant Biol. 57:303–33
    [Google Scholar]
  29. 29.
    Haupt S, Oparka KJ, Sauer N, Neumann S. 2001. Macromolecular trafficking between Nicotiana tabacum and the holoparasite Cuscuta reflexa. J. Exp. Bot. 52:173–77
    [Google Scholar]
  30. 30.
    Hettenhausen C, Li J, Zhuang H, Sun H, Xu Y et al. 2017. Stem parasitic plant Cuscuta australis (dodder) transfers herbivory-induced signals among plants. PNAS 114:E6703–9Demonstrated that dodder transmits ecologically meaningful defensive systemic signals among host plants.
    [Google Scholar]
  31. 31.
    Hilleary R, Gilroy S. 2018. Systemic signaling in response to wounding and pathogens. Curr. Opin. Plant Biol. 43:57–62
    [Google Scholar]
  32. 32.
    Hosford RM Jr. 1967. Transmission of plant viruses by dodder. Bot. Rev. 33:387–406
    [Google Scholar]
  33. 33.
    Hu L. 2021. Integration of multiple volatile cues into plant defense responses. New Phytol. 233:618–23
    [Google Scholar]
  34. 34.
    Jhu M-Y, Sinha NR. 2022. Parasitic plants: an overview of mechanisms by which plants perceive and respond to parasites. Annu. Rev. Plant Biol. 73:433–55
    [Google Scholar]
  35. 35.
    Jiang F, Jeschke WD, Hartung W. 2004. Abscisic acid (ABA) flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite abscisic acid relations. J. Exp. Bot. 55:2323–29
    [Google Scholar]
  36. 36.
    Jiang F, Veselova S, Veselov D, Kudoyarova G, Jeschke WD, Hartung W. 2005. Cytokinin flows from Hordeum vulgare to the hemiparasite Rhinanthus minor and the influence of infection on host and parasite cytokinins relations. Funct. Plant Biol. 32:619–29
    [Google Scholar]
  37. 37.
    Jiang L, Qu F, Li Z, Doohan D. 2013. Inter-species protein trafficking endows dodder (Cuscuta pentagona) with a host-specific herbicide-tolerant trait. New Phytol. 198:1017–22
    [Google Scholar]
  38. 38.
    Jiang Z, Zhao Q, Bai R, Yu R, Diao P et al. 2021. Host sunflower-induced silencing of parasitism-related genes confers resistance to invading Orobanche cumana. Plant Physiol. 185:424–40
    [Google Scholar]
  39. 39.
    Johnson D, Gilbert L. 2015. Interplant signalling through hyphal networks. New Phytol. 205:1448–53
    [Google Scholar]
  40. 40.
    Johnson NR, dePamphilis CW, Axtell MJ 2019. Compensatory sequence variation between trans-species small RNAs and their target sites. eLife 8:e49750
    [Google Scholar]
  41. 41.
    Kehr J. 2006. Phloem sap proteins: their identities and potential roles in the interaction between plants and phloem-feeding insects. J. Exp. Bot. 57:767–74
    [Google Scholar]
  42. 42.
    Kehr J, Morris RJ, Kragler F. 2022. Long-distance transported RNAs: from identity to function. Annu. Rev. Plant Biol. 73:457–74
    [Google Scholar]
  43. 43.
    Kim E-D, Sung S 2012. Long noncoding RNA: unveiling hidden layer of gene regulatory networks. Trends Plant Sci. 17:16–21
    [Google Scholar]
  44. 44.
    Kim G, LeBlanc ML, Wafula EK, dePamphilis CW, Westwood JH 2014. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345:808–11Demonstrated that dodder exchanges large numbers of mobile mRNAs with host plants.
    [Google Scholar]
  45. 45.
    Koch A, Wassenegger M. 2021. Host-induced gene silencing—mechanisms and applications. New Phytol. 231:54–59
    [Google Scholar]
  46. 46.
    Lehtonen P, Helander M, Wink M, Sporer F, Saikkonen K. 2005. Transfer of endophyte-origin defensive alkaloids from a grass to a hemiparasitic plant. Ecol. Lett. 8:1256–63
    [Google Scholar]
  47. 47.
    Lei Y, Xu Y, Zhang J, Song J, Wu J. 2021. Herbivory-induced systemic signals are likely to be evolutionarily conserved in euphyllophytes. J. Exp. Bot. 72:7274–84
    [Google Scholar]
  48. 48.
    Lewsey MG, Hardcastle TJ, Melnyk CW, Molnar A, Valli A et al. 2016. Mobile small RNAs regulate genome-wide DNA methylation. PNAS 113:E801–10
    [Google Scholar]
  49. 49.
    Li L, Li C, Lee GI, Howe GA. 2002. Distinct roles for jasmonate synthesis and action in the systemic wound response of tomato. PNAS 99:6416–21
    [Google Scholar]
  50. 50.
    Li S, Castillo-Gonzalez C, Yu B, Zhang X. 2017. The functions of plant small RNAs in development and in stress responses. Plant J. 90:654–70
    [Google Scholar]
  51. 51.
    Li S, Zhang J, Liu H, Liu N, Shen G et al. 2020. Dodder-transmitted mobile signals prime host plants for enhanced salt tolerance. J. Exp. Bot. 71:1171–84
    [Google Scholar]
  52. 52.
    Liu N, Shen G, Xu Y, Liu H, Zhang J et al. 2020. Extensive inter-plant protein transfer between Cuscuta parasites and their host plants. Mol. Plant 13:573–85Revealed that many proteins in relatively large quantities traveled between host and dodder and between dodder-connected hosts.
    [Google Scholar]
  53. 53.
    Lucas WJ, Bouché-Pillon S, Jackson DP, Nguyen L, Baker L et al. 1995. Selective trafficking of KNOTTED1 homeodomain protein and its mRNA through plasmodesmata. Science 170:1980–83
    [Google Scholar]
  54. 54.
    Mauch-Mani B, Baccelli I, Luna E, Flors V. 2017. Defense priming: an adaptive part of induced resistance. Annu. Rev. Plant Biol. 68:485–512
    [Google Scholar]
  55. 55.
    Molnar A, Melnyk CW, Bassett A, Hardcastle TJ, Dunn R, Baulcombe DC. 2010. Small silencing RNAs in plants are mobile and direct epigenetic modification in recipient cells. Science 328:872–75
    [Google Scholar]
  56. 56.
    Nickrent DL. 2020. Parasitic angiosperms: How often and how many?. Taxon 69:5–27
    [Google Scholar]
  57. 57.
    Nogia P, Pati PK. 2021. Plant secondary metabolite transporters: diversity, functionality, and their modulation. Front. Plant Sci. 12:758202
    [Google Scholar]
  58. 58.
    Notaguchi M, Okamoto S. 2015. Dynamics of long-distance signaling via plant vascular tissues. Front. Plant Sci. 6:161
    [Google Scholar]
  59. 59.
    Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y. 2017. Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nat. Plants 3:17029
    [Google Scholar]
  60. 60.
    Parniske M. 2008. Arbuscular mycorrhiza: the mother of plant root endosymbioses. Nat. Rev. Microbiol. 6:763–75
    [Google Scholar]
  61. 61.
    Paultre DS, Gustin MP, Molnar A, Oparka KJ. 2016. Lost in transit: long-distance trafficking and phloem unloading of protein signals in Arabidopsis homografts. Plant Cell 28:2016–25
    [Google Scholar]
  62. 62.
    Qin Y, Zhang J, Hettenhausen C, Liu H, Li S et al. 2019. The host jasmonic acid pathway regulates the transcriptomic changes of dodder and host plant under the scenario of caterpillar feeding on dodder. BMC Plant Biol. 19:540
    [Google Scholar]
  63. 63.
    Roney JK, Khatibi PA, Westwood JH. 2007. Cross-species translocation of mRNA from host plants into the parasitic plant dodder. Plant Physiol. 143:1037–43
    [Google Scholar]
  64. 64.
    Shahid S, Kim G, Johnson NR, Wafula E, Wang F et al. 2018. MicroRNAs from the parasitic plant Cuscuta campestris target host messenger RNAs. Nature 553:82–85Identified that many dodder microRNAs can move across the haustorial interface and target host mRNAs for degradation.
    [Google Scholar]
  65. 65.
    Shen G, Liu N, Zhang J, Xu Y, Baldwin IT, Wu J. 2020. Cuscuta australis (dodder) parasite eavesdrops on the host plants' FT signals to flower. PNAS 117:23125–30Revealed that the host flowering signal FT protein can travel into dodder to activate dodder flowering.
    [Google Scholar]
  66. 66.
    Smith JD, Woldemariam MG, Mescher MC, Jander G, De Moraes CM. 2016. Glucosinolates from host plants influence growth of the parasitic plant Cuscuta gronovii and its susceptibility to aphid feeding. Plant Physiol. 172:181–97Revealed that dodder could obtain secondary metabolites from hosts for its own defenses.
    [Google Scholar]
  67. 67.
    Song J, Bian J, Xue N, Xu Y, Wu J 2022. Inter-species mRNA transfer among green peach aphids, dodder parasites, and cucumber host plants. Plant Divers. 44:1–10
    [Google Scholar]
  68. 68.
    Song YY, Simard SW, Carroll A, Mohn WW, Zeng RS. 2015. Defoliation of interior Douglas-fir elicits carbon transfer and stress signalling to ponderosa pine neighbors through ectomycorrhizal networks. Sci. Rep. 5:8495
    [Google Scholar]
  69. 69.
    Song YY, Wang M, Zeng R, Groten K, Baldwin IT. 2019. Priming and filtering of antiherbivore defences among Nicotiana attenuata plants connected by mycorrhizal networks. Plant Cell Environ 42:2945–61
    [Google Scholar]
  70. 70.
    Song YY, Ye M, Li C, He X, Zhu-Salzman K et al. 2014. Hijacking common mycorrhizal networks for herbivore-induced defence signal transfer between tomato plants. Sci. Rep. 4:3915
    [Google Scholar]
  71. 71.
    Song YY, Ye M, Li CY, Wang RL, Wei XC et al. 2013. Priming of anti-herbivore defense in tomato by arbuscular mycorrhizal fungus and involvement of the jasmonate pathway. J. Chem. Ecol. 39:1036–44
    [Google Scholar]
  72. 72.
    Song YY, Zeng RS, Xu JF, Li J, Shen X, Yihdego WG. 2010. Interplant communication of tomato plants through underground common mycorrhizal networks. PLOS ONE 5:e13324Discovered that CMNs transfer pathogen infection–induced mobile signals between different plants.
    [Google Scholar]
  73. 73.
    Spallek T, Melnyk CW, Wakatake T, Zhang J, Sakamoto Y et al. 2017. Interspecies hormonal control of host root morphology by parasitic plants. PNAS 114:5283–88Demonstrated that cytokinin derived from the hemiparasitic plant Phtheirospermum japonicum is involved in inducing hypertrophy in Arabidopsis roots.
    [Google Scholar]
  74. 74.
    Su H-J, Hu J-M, Anderson FE, Der JP, Nickrent DL. 2015. Phylogenetic relationships of Santalales with insights into the origins of holoparasitic Balanophoraceae. Taxon 64:491–506
    [Google Scholar]
  75. 75.
    Sun G, Xu Y, Liu H, Sun T, Zhang J et al. 2018. Large-scale gene losses underlie the genome evolution of parasitic plant Cuscuta australis. Nat. Commun. 9:2683
    [Google Scholar]
  76. 76.
    Svetlikova P, Hajek T, Tesitel J. 2015. Hydathode trichomes actively secreting water from leaves play a key role in the physiology and evolution of root-parasitic rhinanthoid Orobanchaceae. Ann. Bot. 116:61–68
    [Google Scholar]
  77. 77.
    Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46
    [Google Scholar]
  78. 78.
    Takahashi F, Suzuki T, Osakabe Y, Betsuyaku S, Kondo Y et al. 2018. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature 556:235–38
    [Google Scholar]
  79. 79.
    Tamiru M, Hardcastle TJ, Lewsey MG. 2018. Regulation of genome-wide DNA methylation by mobile small RNAs. New Phytol. 217:540–46
    [Google Scholar]
  80. 80.
    Thieme CJ, Rojas-Triana M, Stecyk E, Schudoma C, Zhang W et al. 2015. Endogenous Arabidopsis messenger RNAs transported to distant tissues. Nat. Plants 1:15025
    [Google Scholar]
  81. 81.
    Tomilov AA, Tomilova NB, Wroblewski T, Michelmore R, Yoder JI. 2008. Trans-specific gene silencing between host and parasitic plants. Plant J. 56:389–97
    [Google Scholar]
  82. 82.
    Voinnet O, Baulcombe DC. 1997. Systemic signalling in gene silencing. Nature 389:553
    [Google Scholar]
  83. 83.
    Wang N-Q, Kong C-H, Wang P, Meiners SJ 2021. Root exudate signals in plant–plant interactions. Plant Cell Environ. 44:1044–58
    [Google Scholar]
  84. 84.
    Weiberg A, Wang M, Lin FM, Zhao H, Zhang Z et al. 2013. Fungal small RNAs suppress plant immunity by hijacking host RNA interference pathways. Science 342:118–23
    [Google Scholar]
  85. 85.
    Westwood JH, Yoder JI, Timko MP, dePamphilis CW. 2010. The evolution of parasitism in plants. Trends Plant Sci. 15:227–35
    [Google Scholar]
  86. 86.
    Wu J, Baldwin IT. 2010. New insights into plant responses to the attack from insect herbivores. Annu. Rev. Genet. 44:1–24
    [Google Scholar]
  87. 87.
    Wu Y, Luo D, Fang L, Zhou Q, Liu W, Liu Z. 2022. Bidirectional lncRNA transfer between Cuscuta parasites and their host plant. Int. J. Mol. Sci. 23:561
    [Google Scholar]
  88. 88.
    Yang L, Perrera V, Saplaoura E, Apelt F, Bahin M et al. 2019. m5C methylation guides systemic transport of messenger RNA over graft junctions in plants. Curr. Biol. 29:2465–76.e5
    [Google Scholar]
  89. 89.
    Yazaki K. 2005. Transporters of secondary metabolites. Curr. Opin. Plant Biol. 8:301–7
    [Google Scholar]
  90. 90.
    Yoshida S, Cui S, Ichihashi Y, Shirasu K. 2016. The haustorium, a specialized invasive organ in parasitic plants. Annu. Rev. Plant Biol. 67:643–67
    [Google Scholar]
  91. 91.
    Zhang J, Xu Y, Xie J, Zhuang H, Liu H et al. 2021. Parasite dodder enables transfer of bidirectional systemic nitrogen signals between host plants. Plant Physiol. 185:1395–410
    [Google Scholar]
  92. 92.
    Zhang W, Thieme CJ, Kollwig G, Apelt F, Yang L et al. 2016. tRNA-related sequences trigger systemic mRNA transport in plants. Plant Cell 28:1237–49
    [Google Scholar]
  93. 93.
    Zhang YC, Zou YN, Liu LP, Wu QS. 2019. Common mycorrhizal networks activate salicylic acid defense responses of trifoliate orange (Poncirus trifoliata). J. Integr. Plant Biol. 61:1099–111
    [Google Scholar]
  94. 94.
    Zhang Z, Zheng Y, Ham B-K, Chen J, Yoshida A et al. 2016. Vascular-mediated signalling involved in early phosphate stress response in plants. Nat. Plants 2:16033
    [Google Scholar]
  95. 95.
    Zhuang H, Li J, Song J, Hettenhausen C, Schuman MC et al. 2018. Aphid (Myzus persicae) feeding on the parasitic plant dodder (Cuscuta australis) activates defense responses in both the parasite and soybean host. New Phytol. 218:1586–96
    [Google Scholar]
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