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Sirangelo, T.M.; Ludlow, R.A.; Spadafora, N.D. Potential Pathogen Resistance in Cannabis sativa. Encyclopedia. Available online: https://encyclopedia.pub/entry/48339 (accessed on 22 June 2024).
Sirangelo TM, Ludlow RA, Spadafora ND. Potential Pathogen Resistance in Cannabis sativa. Encyclopedia. Available at: https://encyclopedia.pub/entry/48339. Accessed June 22, 2024.
Sirangelo, Tiziana M., Richard A. Ludlow, Natasha D. Spadafora. "Potential Pathogen Resistance in Cannabis sativa" Encyclopedia, https://encyclopedia.pub/entry/48339 (accessed June 22, 2024).
Sirangelo, T.M., Ludlow, R.A., & Spadafora, N.D. (2023, August 22). Potential Pathogen Resistance in Cannabis sativa. In Encyclopedia. https://encyclopedia.pub/entry/48339
Sirangelo, Tiziana M., et al. "Potential Pathogen Resistance in Cannabis sativa." Encyclopedia. Web. 22 August, 2023.
Potential Pathogen Resistance in Cannabis sativa
Edit

Cannabis (Cannabis sativa L.) is one of the earliest cultivated crops, valued for producing a broad spectrum of compounds used in medicinal products and being a source of food and fibre.

Cannabis pathogen resistance omics genome editing

1. Introduction

Cannabis (Cannabis sativa L.) is a dicotyledonous angiosperm originating from Central Asia but is cultivated across many parts of the world due to its ability to grow in a wide range of habitats and environmental conditions [1].
Cannabis belongs to the Cannabaceae family and is considered one of the earliest cultivated crops, being of particular interest due to its multiple uses. Cannabinoids are responsible for the pharmacological and psychoactive properties of this crop, and these therapeutic characteristics have drawn the attention of researchers from all over the world. Additionally, hemp, a Cannabis variety containing less than 0.3% of tetrahydrocannabinol (THC), is cultivated for biomass and fibre, which constitute feedstock for industrial uses. Conversely, medicinal Cannabis contains a greater amount of THC, which has been increasing in recent years, reaching 17–28% of the dry weight in some varieties [2], or even exceeding 30% in others [3].
Among the ~130 secondary metabolites identified in Cannabis [4], THC, along with cannabidiol (CBD), constitute the most relevant compounds produced by this crop and are the main focus of Cannabis breeding programs.
Breeding efforts to produce Cannabis with unique fragrance and flavour characteristics are also of interest. Consequently, the profile of terpenoids, which are highly abundant and largely responsible for the characteristic aroma of Cannabis, is of importance, with isoprenes, monoterpenes, and sesquiterpenes being the predominant classes [5][6].
Due to the legislation regulating Cannabis and related breeding programs, research into the cannabinoid biosynthetic pathway is underrepresented, and it has not been sufficiently characterised, especially at the molecular level [5][7]. Many other major crops have already been widely investigated from this perspective, especially after the advent of Next Generation Sequencing (NGS) technologies [7]. However, the recent modifications in legislation and less stringent regulations [8], as well as the availability of the Cannabis genomic sequence [9], have broadened research in this crop, with the aim also to improve its biomass quality, in the context of sustainable agriculture [10][11].
These legislative changes have also resulted in increased Cannabis production and, with it, a growth of the incidence and severity of crop pathogens, along with the detection of previously unreported diseases. Among emerging pathogens of Cannabis recently reported there are Botrytis cinerea [12][13], Fusarium spp. [14][15], Pythium [16][17] Golovinomyces spp. [12][13], and Hop latent viroid [18], where hop (Humulus lupulus) is a member of Cannabaceae and is closely related to Cannabis [19]. These pathogens can be grouped according to the tissues they infect: root and crown (Fusarium oxysporum, Fusarium proliferatum, Fusarium solani, Pythium myriotylum, Pythium dissotocum, Pythium aphanidermatum), leaves (Golovinomyces spp.), buds (Hop latent viroid) [12]. Botrytis cinerea is often classified as a postharvest pathogen and can attack Cannabis seeds, leaves, and stalks [12]. Fusarium and Pythium species are the most destructive root pathogens, especially when the infection occurs during vegetative growth. Crop losses resulting from the attack of these two pathogens can reach 30% of the total yield [12]. Botryis and Fusarium species also are harmful, as well as other fungi, such as Golovinomyces species, causing powdery mildew (PM, a common term for several taxa of plant pathogenic fungi), and colonizing foliar and flower tissues through the production of spores. Furthermore, extensive infection by fungi such as Fusarium can lead to mycotoxin accumulation in the tissues, potentially harmful to human health [20]. Hop latent viroid leads to malformation of buds and can infect other parts of the crop [18].
The above-reported fungi, oomycetes and the mentioned viroid have been investigated in Cannabis, as well as in several other crops, but little is known about infection within the seed, even though there are harmful pathogens, such as Alternaria, which can start their attack in developing seedlings [12]. The lack of significant research results on Cannabis bacteria pathogen defence mechanisms has also been underlined [21].
On the other hand, research into the characterization and use of biocontrol agents has consistently improved in recent years [22]. The use of synthetic fungicides to control fungal diseases has limitations due to toxicological risks, and it is necessary to replace them with safer means, for human health and with reduced environmental risks. Omics methods and their applications in the biocontrol field were recently reviewed by Massart et al. [23]. A better understanding of the molecular mechanisms underlying pathogen plant resistance can only have positive effects in this field of research.
Many of the above-reported pathogens have been identified using methods based on Polymerase Chain Reaction (PCR) of parts of rDNA, such as Internal Transcribed Spacer (ITS) and Inter Generic Spacer (IGS) regions [24]. However, for Golovinomyces and Botrytis, additional molecular markers were necessary to differentiate between species [25][26].
Abbreviations used throughout the manuscript are listed in Table 1.
Table 1. List of abbreviations used in this entry.

Abbreviations

Definition

ABA

abscisic acid

BR

Brassinosteroids

CBD

Cannabidiol

CRISPR/Cas9

Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-Associated Protein

ERF

Ethylene Response Factor

ET

Ethylene

ETI

Effector-Triggered Immunity

IGS

Inter Generic Spacer

ITS

Internal Transcribed Spacer

JA

Jasmonic Acid

JAZ

JA-Zim

LRR

Leucine-Rich Repeat

MAPK

Mitogen-Activated Protein Kinase

NBS

Nucleotide Binding Site

NGS

Next Generation Sequencing

NHR

Non Host Resistance

NO

Nitric Oxide

PAL

Phenylalanine Ammonia-Lyase

PAMPs

Pathogen-Associated Molecular Patterns

PM

Powdery Mildew

PR

Pathogenesis-Related protein

PRRs

Pattern Recognition Receptors

PTI

PAMP-Triggered Immunity

PCR

Polymerase Chain Reaction

PCWDEs

Plant Cell Wall Degrading Enzymes

R genes

Resistance genes

RLK

Receptor-Like Kinases

ROS

Reactive Oxygen Species

S genes

Susceptibility genes

SA

Salicylic Acid

SNP

Single Nucleotide Polymorphism

THC

Tetrahydrocannabinol

TLP

Thaumatin-Like Protein

2. Overview of Cannabis Resistance Genes to Pathogens

Cannabis includes genotypes whose origins are geographically very different [27], and this genetic diversity leads us to believe the existence of naturally occurring genotypes characterised by resistance to specific pathogens. Indeed, among 12 Cannabis genotypes evaluated, it was found that seven displayed partial or complete resistance to PM [28]. Furthermore, a recent study provided insight on the variability of Cannabis cultivars on disease resistance and cannabinoid accumulation over the course of crop maturation [29]. Here, PM resistance was shown for ‘FL 58’ cultivar, on which PM was never observed, as well as ‘RN13a’, ‘Otto II’, and ‘AC/DC’, cultivars, showing very low levels of PM disease.
Studies on other crop species have investigated the molecular mechanisms of resistance to Fusarium and PM [30][31], providing insights for further research on disease resistance responses in Cannabis. Conversely, the search for Cannabis resistance traits to viral pathogens did not yield answers so quickly [32].
Several studies focused on non-host resistance (NHR), a resistance of plant species against all non-adapted pathogens, which is considered the most durable and efficient immune system of plants, as described in the review by Oh and Choi [33]. Most non-adapted pathogen attacks are stopped by an innate defence response based on the recognition of pathogen-associated molecular patterns (PAMPs) by the plant pattern recognition receptors (PRRs), which activates PAMP-triggered immunity (PTI), also induced by reactive oxygen species (ROS) production and mitogen-activated protein kinase (MAPK) [34]. Specific PAMPs, harpin and flg22, were analyzed to study the response to Pythium in Cannabis [35]. Results showed that harpin-enhanced hemp seedlings resistant to Pythium aphanidermatum, while flg22 did not contribute to the defence mechanism against P. aphanidermatum. The lack of comprehensive experimental evidence supporting the recognition of PAMPs in Cannabis opens a field of future research.
The salicylic acid (SA) or the jasmonic acid (JA)/ethylene (ET) signalling pathways, which are known to have an antagonistic interaction [36], are also involved in the activation of disease resistance mechanisms. SA is involved in several key components of plant defence through complex networks, generally activated by biotrophic pathogens, and JA/ET signalling pathways are usually required for the activation of plant defence against necrotrophic pathogens [36].
However, specialised pathogens can suppress PTI responses through effector proteins, which can, in turn, activate subsequent defence responses called effector-triggered immunity (ETI) in plants with immunity to a specialised pathogen. ETI is also activated by SA or JA/ET pathway [37]. An ETI response is generally able to control specific pathogen attacks [38]. The majority of disease resistance genes in plants encode the conserved nucleotide binding site-leucine-rich repeat (NBS-LRR) disease resistance proteins [39][40], which can identify specific effectors to trigger ETI [37][41].
Studies on Wall-Associated receptor Kinases (WAKs) and WAK-like (WAKLs) genes have underlined their role in pathogen resistance across a wide range of plants [42]. The Arabidopsis WAKL22 gene is the homolog of Cannabis WAK7 and was shown to be responsible for dominant resistance against several Fusarium strains [43]. The cotton WAK18 and WAK29 (homolog of CsWAK4 and CsWAK7, respectively), specifically expressed in flowers, showed pathogen resistance characteristics [44]. The Juglans regia WAK9, the homolog of CsWAK1, has been demonstrated to be involved in pathogen response [45]. A recent analysis of the WAK gene family in Cannabis sativa investigated some CsWAKs/CsWAKLs (CsWAK1, CsWAK4, CsWAK7, CsWAKL1, and CsWAKL7) in leaf tissues, showing how their expression differs from their homologs in other plants [46]. Furthermore, the hemp WAK1 gene is highly expressed under drought stress conditions, and its expression can be induced by phytohormones like salicylic acid, methyl jasmonate, and ethylene [47]. These findings put the bases for future research on the potential roles of CsWAK/CsWAKLs in response to hormone treatments and abiotic/biotic stresses, including pathogen attacks.
Biosynthesis of specific terpenes may affect biotic and abiotic stress plant response and disease resistance [48]. For instance, few studies showed that while phytoanticipins terpenes are constitutively secreted in the absence of plant pathogen infection, phytoalexins are produced in response to pathogenic microbes [48][49]. A whole genome resequencing data across diverse samples of feral and domesticated lineages of C. sativa, aimed to examine their population structure, also allowed the identification of 6 loci related to stress response and 1 gene potentially involved in disease resistance [50]. This gene was annotated as mevalonate kinase (MEV kinase) and is involved in sesquiterpenes biosynthesis via the mevalonic acid pathway, with sesquiterpenes known for their antifungal properties [51]. Despite successful breeding efforts to modify terpene profiles, plant pathogens still constitute a significant cause of crop loss in Cannabis production [52].

3. Genome Editing to Generate Disease-Resistant Cannabis Varieties

Omics approaches are comprehensive methods for investigating defence response pathways and have been used broadly in medicinal plants [53][54]. Furthermore, by identifying candidate resistance genes and yielding an in-depth knowledge of the underlying molecular mechanism, they provide a strong basis for genome editing studies to generate disease-resistant Cannabis varieties [54].
The use of genetic engineering methods in Cannabis to enhance its resistance to pathogens and to improve desirable traits is a subject of investigation in several research projects [55]. However, it is challenging to regenerate fully developed Cannabis transgenic plants [56], and, despite some candidate genes involved in pathogen resistance having been identified, functions of these genes are not yet fully validated, and only a few studies report stable transformation for Cannabis tissues [43].
The first edited Cannabis line was developed by Agrobacterium-mediated transformation [57], in which overexpressing the Cannabis developmental regulator chimera in the embryo hypocotyls of unripe grains increased the regeneration efficiency. By applying this method, the development of transgenic callus from Cannabis has been achieved [58]. Evidence suggests that the overexpression of Non-expressor of Pathogenesis-Related genes-1 (NPR1) in Arabidopsis can confer disease resistance to different pathogens in various plants, such as cotton [59] and Brassica juncea [60]. The AtNPR1 gene has been introduced into C. sativa and confirmed by PCR and RT-PCR, showing that Cannabis can be transformed to generate disease-resistant varieties [60].
A recent mini-review on hemp genome editing [61] discusses the opportunity offered by next-generation genome editing technology. The direct delivery of CRISPR/Cas (Clustered Regularly Interspaced Short Palindromic Repeats/CRISPR-Associated Protein) ribonucleoprotein complexes into plant tissue overcomes the drawback of Agrobacterium-mediated transformation, by which external plasmid DNA is introduced into the crop genome. CRISPR/Cas technology, which is still less commonly used in Cannabis, can be applied to introduce a specific DNA fragment to a precise location in the genome. It could have broad applications in Cannabis breeding, modifying gene regulation and developing pathogen-resistant plants, as already performed in other recalcitrant plants, such as grapes [61]. For instance, a protocol for this type of transformation in C. sativa was developed, and genome-edited Cannabis was produced by CRISPR/Cas9 approach [61].
By using CRISPR/Cas9, the previously discussed results of the study of Mihalyov and Garfinkel [62], consisting of a set of R candidate genes, could be used as target genes to improve PM resistance in the crop.
Furthermore, results reported in other plants could provide useful inputs for Cannabis gene editing. For instance, the genetic transformation of wheat with TLP and glucanases resulted in enhanced resistance to Fusarium [63], and MLO-7 was used as a host susceptibility (S) gene to improve grapevine and apple disease resistance to PM [64].
Overall, this advanced genome editing approach, based on a transgene-free framework, can address many problems associated with transgenic-based approaches and could be applied to produce improved non-transgenic Cannabis, with the most industrially desirable traits, including pathogen resistance traits.
Another alternative to Agrobacterium transformation protocol is represented by the use of a nanoparticle-based transient gene; through this method, multiple gene plasmids were expressed simultaneously in Cannabis leaf cells [65]. However, the study of disease resistance through this method is still in its infancy. It offers promising new perspectives in regulating the content of secondary metabolites, inducing pathogen resistance genes, and obtaining transgenic disease-resistant plants [66][67].
On this basis, there is a real possibility to improve Cannabis disease resistance by acting on targeted R genes or on S genes. A deep understanding of the underlying molecular mechanisms in which they are involved, as well as of plant-pathogen interactions, and the application of innovative molecular techniques is leading to innovations in the development of pathogen-resistant plants [68].
To date, it is still challenging to produce transgenic or gene-edited Cannabis, but the previously reported studies, and several gene editing approaches applied in other plant species, constitute good reference points for further Cannabis resistance research.
To date, few Cannabis omics studies are focused on its defence mechanisms against pathogens and the associated resistance genes. However, these studies, along with omics investigations of disease resistance molecular mechanisms in other crops (see Table 2), could constitute a suitable starting point for further Cannabis research in this field, especially if combined with gene editing approaches which have recently made significant progress, opening new perspectives in regulating the content of secondary metabolites and inducing pathogen resistance genes.
Table 2. Table summarizing the main studies examined in this entry.

Pathogen

Crop

Resistance Genes/Gene Families and Proteins

References

PM, Fusarium, Botrytis cinerea, Pythium

Cannabis

-

[12]

PM-Golovinomyces spp.

Hops

Genes encoding NBS proteins

[69]

PM-Golovinomyces spp.

Cannabis

R gene, designated as PM1

[62]

PM-Golovinomyces spp.

Cannabis

Genes encoding NBS-LRR proteins

[62]

F. oxysporum

Arabidopsis

Genes encoding JA and P450 proteins

[70]

F. oxysporum

Resistant

crops

Genes encoding 4-coumarate-CoA ligase, polyphenol oxidase, cellulose synthase

[71]

F. oxysporum

Arabidopsis

WAK gene family, genes encoding RLKs, WRKY, ERF, MYB, and NAC TFs

[72]

F. oxysporum

Arabidopsis

Genes encoding dirigent-like protein, CAP family and wound-responsive family proteins, some ERF TFs

[73]

F. oxysporum

Cannabis

WAK7

[46]

Fusarium spp.

Cannabis

-

[74]

Botrytis cinerea

Other crops

PRs, SA, JA, ET, ABA and BR gene family

[75][76]

Botrytis cinerea

Cannabis

Genes involved in JA/ET, HEL, PAL, SA, PR1 and PR2 pathways

[77]

Pythium

Other crops

Flg22 and PTI in plants

[78]

Pythium

Cannabis

Harpin and Flg22 PAMPs

[35]

References

  1. Clarke, R.C.; Merlin, M.D. Cannabis domestication, breeding history, present day genetic diversity, and future prospects. Crit. Rev. Plant Sci. 2016, 35, 293–327.
  2. Stuyt, E. The problem with the current high potency THC marijuana from the perspective of an addiction psychiatrist. Mo. Med. 2018, 115, 482–486.
  3. Schwabe, A.L.; Johnson, V.; Harrelson, J.; McGlaughlin, M.E. Uncomfortably high: Testing reveals inflated THC potency on retail Cannabis labels. PLoS ONE 2023, 18, e0282396.
  4. Morales, P.; Hurst, D.P.; Reggio, P.H. Molecular targets of the phytocannabinoids: A complex picture. Prog. Chem. Org. Nat. Prod. 2017, 103, 103–131.
  5. Sirangelo, T.M.; Ludlow, R.A.; Spadafora, N.D. Multi-Omics approaches to study molecular mechanisms in Cannabis sativa. Plants 2022, 11, 2182.
  6. Chandra, S.; Lata, H.; Khan, I.A.; Elsohly, M.A. Cannabis sativa L.: Botany and horticulture. In Cannabis sativa L.—Botany and Biotechnology; Chandra, S., Lata, H., Elsohly, M.A., Eds.; Springer: Cham, Switzerland, 2017; pp. 79–100.
  7. Hurgobin, B.; Tamiru-Oli, M.; Welling, M.T.; Doblin, M.S.; Bacic, A.; Whelan, J.A.; Lewsey, M.G. Recent advances in Cannabis sativa genomics research. N. Phytol. 2020, 230, 73–89.
  8. Pacula, R.L.; Smart, R. Medical marijuana and marijuana legalization. Ann. Rev. Clin. Psychol. 2017, 13, 397–419.
  9. Gao, S.; Wang, B.; Xie, S.; Xu, X.; Zhang, J.; Pei, L.; Yu, Y.; Yang, W.; Zhang, Y. A high quality reference genome of wild Cannabis sativa. Hortic. Res. 2020, 7, 73.
  10. Petit, J.; Salentijn, E.M.J.; Paulo, M.J.; Denneboom, C.; van Loo, E.N.; Trindade, L.M. Elucidating the genetic architecture of fiber quality in hemp (Cannabis sativa L.) using a Genome-Wide Association study. Front. Genet. 2020, 11, 566314.
  11. Sirangelo, T.M.; Ludlow, R.A.; Chenet, T.; Pasti, L.; Spadafora, N.D. Multi-Omics and genome editing studies on plant cell walls to improve biomass quality. Agriculture 2023, 13, 752.
  12. Punja, Z.K. Emerging diseases of Cannabis sativa and sustainable management. Pest Manag. Sci. 2021, 77, 3857–3870.
  13. Punja, Z.K.; Collyer, D.; Scott, C.; Lung, S.; Holmes, J.; Sutton, D. Pathogens and molds affecting production and quality of Cannabis sativa L. Front. Plant Sci. 2019, 10, 1120.
  14. McCain, A.H.; Noviello, C. Biological control of Cannabis sativa. In Proceedings of the VI International Symposium on Biological Control of Weeds, Vancouver, WA, Canada, 19–25 August 1984; Delfosse, E.S., Ed.; Agricultural Canada: Ottawa, ON, Canada, 1985; pp. 635–642.
  15. Punja, Z.K. Epidemiology of Fusarium oxysporum causing root and crown rot of Cannabis (Cannabis sativa L., marijuana) plants in commercial greenhouse production. Can. J. Plant Pathol. 2020, 43, 216–235.
  16. Cheng, Y.; Tang, X.; Gao, C.; Li, Z.; Chen, J.; Guo, L.; Wang, T.; Xu, J. Molecular diagnostics and pathogenesis of fungal pathogens on bast fiber crops. Pathogens 2020, 9, 223.
  17. Punja, Z.K.; Rodriguez, G. Fusarium and Pythium species infecting roots of hydroponically grown marijuana (Cannabis sativa L.) plants. Can. J. Plant Pathol. 2018, 40, 498–513.
  18. Warren, J.G.; Mercado, J.; Grace, D. Occurrence of hop latent viroid causing disease in Cannabis sativa in California. Plant Dis. 2019, 103, 2699.
  19. Wolfenbarger, S.N.; Massie, S.T.; Ocamb, C.; Eck, E.B.; Grove, G.G.; Nelson, M.E.; Probst, C.; Twomey, M.C.; Gent, D.H. Distribution and characterization of Podosphaera macularis virulent on hop cultivars possessing R6-Based resistance to Powdery Mildew. Plant Dis. 2016, 100, 1212–1221.
  20. Desjardins, A.E. Fusarium Mycotoxins: Chemistry, Genetics, and Biology; APS Press: St. Paul, MN, USA, 2006.
  21. Vujanovic, V.; Korber, D.R.; Vujanovic, S.; Vujanovic, J.; Jabaji, S. Scientific prospects for cannabis-microbiome research to ensure quality and safety of products. Microorganisms 2020, 8, 290.
  22. Palmieri, D.; Ianiri, G.; Del Grosso, C.; Barone, G.; De Curtis, F.; Castoria, R.; Lima, G. Advances and perspectives in the use of biocontrol agents against fungal plant diseases. Horticulturae 2022, 8, 577.
  23. Massart, S.; Martinez-Medina, M.; Jijakli, M.H. Biological control in the microbiome era: Challenges and opportunities. Biol. Control 2015, 89, 98–108.
  24. Op De Beeck, M.; Lievens, B.; Busschaert, P.; Declerck, S.; Vangronsveld, J.; Colpaert, J.V. Comparison and validation of some ITS primer pairs useful for fungal metabarcoding studies. PLoS ONE 2014, 9, e97629.
  25. Pépin, N.; Punja, Z.K.; Joly, D.L. Occurrence of powdery mildew caused by Golovinomyces chicoracearum sensu lato on Cannabis sativa in Canada. Plant Dis. 2018, 102, 2644.
  26. Garfinkel, A.R. Three Botrytis species found causing gray mold on industrial hemp (Cannabis sativa) in Oregon. Plant Dis. 2020, 104, 2026.
  27. Punja, Z.K.; Rodriguez, G.; Chen, S. Assessing genetic diversity in Cannabis sativa using molecular approaches. In Cannabis sativa L.-Botany and Biotechnology; Chandra, S., Lata, L., ElSohly, M.A., Eds.; Springer: Berlin, Germany, 2017; pp. 395–418.
  28. Scott, C.; Punja, Z.K. Evaluation of disease management approaches for powdery mildew on Cannabis sativa L. (marijuana) plants. Can. J. Plant Pathol. 2021, 34, 394–412.
  29. Stack, G.M.; Toth, J.A.; Carlson, C.H.; Cala, A.R.; Marrero-González, M.I.; Wilk, R.L.; Gentner, D.R.; Crawford, J.L.; Philippe, G.; Rose, J.K.C. Season-long characterization of high-cannabinoid hemp (Cannabis sativa L.) reveals variation in cannabinoid accumulation, flowering time, and disease resistance. GCB Bioenergy 2021, 13, 546–561.
  30. Bai, Y.; Huang, C.C.; Hulst, R.V.D.; Meijer-Dekens, F.; Bonnema, G.; Lindhout, P. QTLs for tomato powdery mildew resistance (Oidium lycopersici) in Lycopersicon parviflorum G1.1601 localize with two qualitative powdery mildew resistance genes. Mol. Plant Microbe Interact. 2003, 16, 169–176.
  31. Tassone, M.R.; Bagnaresi, P.; Desiderio, F.; Bassolino, L.; Barchi, L.; Florio, F.E.; Sunseri, F.; Sirangelo, T.M.; Rotino, G.L.; Toppino, L. A Genomic BSAseq Approach for the characterization of QTLs underlying resistance to Fusarium oxysporum in eggplant. Cells 2022, 11, 2548.
  32. Nachappa, P.; Fulladolsa, A.C.; Stenglein, M. Wild wild west: Emerging viruses and viroids of hemp. Outlooks Pest Manag. 2020, 31, 175–179.
  33. Oh, S.; Choi, D. Receptor-mediated nonhost resistance in plants. Essays Biochem. 2022, 66, 435–445.
  34. Lee, H.A.; Lee, H.Y.; Seo, E.; Lee, J.; Kim, S.B.; Oh, S.; Choi, E.; Choi, E.; Lee, S.E.; Choi, D. Current understandings of plant nonhost resistance. Mol. Plant-Microbe Interact. 2017, 30, 5–15.
  35. Sands, L.B.; Cheek, T.; Reynolds, J.; Ma, Y.; Berkowitz, G.A. Effects of Harpin and Flg22 on growth enhancement and pathogen defense in Cannabis sativa seedlings. Plants 2022, 11, 1178.
  36. Benjamin, G.; Pandharikar, G.; Frendo, P. Salicylic acid in plant symbioses: Beyond plant pathogen interactions. Biology 2022, 11, 861.
  37. Ding, L.N.; Li, Y.T.; Wu, Y.Z.; Li, T.; Geng, R.; Cao, J.; Zhang, W.; Tan, X.-L. Plant disease resistance-related signaling pathways: Recent progress and future prospects. Int. J. Mol. Sci. 2022, 23, 16200.
  38. Boba, A.; Kostyn, K.; Kozak, B.; Zalewski, I.; Szopa, J.; Kulma, A. Transcriptomic profiling of susceptible and resistant flax seedlings after Fusarium oxysporum lini infection. PLoS ONE 2021, 16, e0246052.
  39. McHale, L.; Tan, X.; Koehl, P.; Michelmore, R.W. Plant NBS-LRR proteins: Adaptable guards. Genome Biol. 2006, 7, 212.
  40. Andolfo, G.; Dohm, J.C.; Himmelbauer, H. Prediction of NB-LRR resistance genes based on full-length sequence homology. Plant J. 2022, 110, 1592–1602.
  41. Xie, S.S.; Duan, C.G. Epigenetic regulation of plant immunity: From chromatin codes to plant disease resistance. aBIOTECH 2023, 1–16.
  42. He, Z.H.; He, D.; Kohorn, B.D. Requirement for the induced expression of a cell wall associated receptor kinase for survival during the pathogen response. Plant J. 1998, 14, 55–63.
  43. Diener, A.C.; Ausubel, F.M. Resistance to Fusarium oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics 2005, 171, 305–321.
  44. Yang, J.; Xie, M.; Wang, X.; Wang, G.; Zhang, Y.; Li, Z.; Ma, Z. Identification of cell wall-associated kinases as important regulators involved in Gossypium hirsutum resistance to Verticillium dahliae. BMC Plant Biol. 2021, 21, 220.
  45. Li, L.; Yu, S.; Chen, J.; Cheng, C.; Sun, J.; Xu, Y.; Deng, C.; Dai, Z.; Yang, Z.; Chen, X.; et al. Releasing the full potential of Cannabis through biotechnology. Agronomy 2022, 12, 2439.
  46. Sipahi, H.; Whyte, T.D.; Ma, G.; Berkowitz, G. Genome-Wide identification and expression analysis of Wall-Associated Kinase (WAK) gene family in Cannabis sativa L. Plants 2022, 11, 2703.
  47. Maravaneh, H.; Davarpanah, S.J. Study of cannabinoids biosynthesis-related genes in hemp (Cannabis sativa L.) under drought stress by in vitro and in silico tools. J. Appl. Biotechnol. Rep. 2022, 9, 504–510.
  48. Ninkuu, V.; Zhang, L.; Yan, J.; Fu, Z.; Yang, T.; Zeng, H. Biochemistry of terpenes and recent advances in plant protection. Int. J. Mol. Sci. 2021, 22, 5710.
  49. Silva, L.N.; Zimmer, K.R.; Macedo, A.J.; Trentin, D.S. Plant natural products targeting bacterial virulence factors. Chem. Rev. 2016, 116, 9162–9236.
  50. Woods, W.; Price, N.; Matthews, P.; McKay, J.K. Genome-wide polymorphism and genic selection in feral and domesticated lineages of Cannabis sativa. G3 2023, 13, jkac209.
  51. Sommano, S.R.; Chittasupho, C.; Ruksiriwanich, W.; Jantrawut, P. The Cannabis terpenes. Molecules 2020, 25, 5792.
  52. Backer, R.; Schwinghamer, T.; Rosenbaum, P.; McCarty, V.; Eichhorn Bilodeau, S.; Lyu, D.; Ahmed, M.B.; Robinson, G.; Lefsrud, M.; Wilkins, O.; et al. Closing the yield gap for Cannabis: A meta-analysis of factors determining Cannabis yield. Front. Plant Sci. 2019, 10, 495.
  53. Amer, B.; Baidoo, E.E.K. Omics-driven biotechnology for industrial applications. Front. Bioeng. Biotechnol. 2021, 9, 613307.
  54. Yang, L.; Yang, Y.; Huang, L.; Cui, X.; Liu, Y. From single- to multi-omics: Future research trends in medicinal plants. Brief. Bioinform. 2023, 24, bbac485.
  55. Punja, Z.K.; Holmes, J.; Collyer, D.; Lung, S. Development of tissue culture methods for marijuana (Cannabis sativa L.) strains to achieve Agrobacterium-mediated transformation to enhance disease resistance. Vitro Cell. Dev. Biol. Anim. 2019, 55, 523.
  56. Feeney, M.; Punja, Z.K. The role of Agrobacterium-mediated and other gene-transfer technologies in Cannabis research and product development, in Cannabis sativa L. In Botany and Biotechnology; Chandra, S., Lata, L., ElSohly, M.A., Eds.; Springer: Berlin, Germany, 2017; pp. 343–363.
  57. Zhang, X.; Xu, G.; Cheng, C.; Lei, L.; Sun, J.; Xu, Y.; Deng, C.; Dai, Z.; Yang, Z.; Chen, X.; et al. Establishment of an Agrobacterium mediated genetic transformation and CRISPR/Cas9-mediated targeted mutagenesis in Hemp (Cannabis sativa L.). Plant Biotechnol. J. 2021, 19, 1979–1987.
  58. Holmes, J.E.; Punja, Z.K. Agrobacterium-mediated transformation of THC-containing Cannabis sativa L. yields a high frequency of transgenic calli expressing bialaphos resistance and non-expressor of PR1 (NPR1) genes. Botany, 2023; in press.
  59. Kumar, V.; Joshi, S.G.; Bell, A.A.; Rathore, K.S. Enhanced resistance against Thielaviopsis basicola in transgenic cotton plants expressing Arabidopsis NPR1 gene. Transgenic Res. 2013, 22, 359–368.
  60. Ali, S.; Mir Zahoor, A.; Tyagi, A.; Mehari, H.; Meena, R.P.; Bhat, J.A.; Yadav, P.; Papalou, P.; Rawat, S.; Grover, A. Overexpression of NPR1 in Brassica juncea confers broad spectrum resistance to fungal pathogens. Front. Plant Sci. 2017, 8, 1693.
  61. Shiels, D.; Prestwich, B.D.; Koo, O.; Kanchiswamy, C.N.; O’Halloran, R.; Badmi, R. Hemp genome editing—Challenges and opportunities. Front. Genome 2022, 4, 823486.
  62. Mihalyov, P.D.; Garfinkel, A.R. Discovery and genetic mapping of PM1, a powdery mildew resistance gene in Cannabis sativa L. Front. Agron. 2021, 3, 720215.
  63. Mackintosh, C.A.; Lewis, J.; Radmer, L.E.; Shin, S.; Heinen, S.J.; Smith, L.A.; Wyckoff, M.N.; Dill-Macky, R.; Evans, C.K.; Kravchenko, S.; et al. Overexpression of defense response genes in transgenic wheat enhances resistance to Fusarium head blight. Plant Cell Rep. 2007, 26, 479–488.
  64. Malnoy, M.; Viola, R.; Jung, M.H.; Koo, O.J.; Kim, S.; Kim, J.S.; Velasco, R.; Nagamangala Kanchiswamy, C. DNA-free genetically edited grapevine and apple protoplast using CRISPR/Cas9 ribonucleoproteins. Front. Plant Sci. 2016, 7, 1904.
  65. Ahmed, S.; Gao, X.; Jahan, M.A.; Adams, M.; Wu, N.; Kovinich, N. Nanoparticle-based genetic transformation of Cannabis sativa. J. Biotechnol. 2021, 326, 48–51.
  66. Dolgin, E. The bioengineering of Cannabis. Nature 2019, 572, 5–7.
  67. Dong, B.R.; Jiang, R.; Chen, J.F.; Xiao, Y.; Lv, Z.Y.; Chen, W.S. Strategic nanoparticle-mediated plant disease resistance. Crit. Rev. Biotechnol. 2022, 43, 22–37.
  68. Tyagi, S.; Kumar, R.; Kumar, V.; Won, S.Y.; Shukla, P. Engineering disease resistant plants through CRISPR-Cas9 technology. GM Crops Food 2021, 12, 125–144.
  69. Padgitt-Cobb, L.K.; Kingan, S.B.; Henning, J.A. Genomic analysis of powdery mildew resistance in a hop (Humulus lupulus L.) bi-parental population segregating for “R6-locus”. Euphytica 2019, 216, 10.
  70. Liu, F.; Jiang, H.; Ye, S.; Chen, W.P.; Liang, W.; Xu, Y.; Sun, B.; Sun, J.; Wang, Q.; Cohen, J.D.; et al. The Arabidopsis P450 protein CYP82C2 modulates jasmonate-induced root growth inhibition, defense gene expression and indole glucosinolate biosynthesis. Celi. Res. 2010, 20, 539–552.
  71. Li, C.Y.; Deng, G.M.; Yang, J.; Viljoen, A.; Jin, Y.; Kuang, R.B.; Zuo, C.W.; Lv, Z.C.; Yang, Q.S.; Sheng, O.; et al. Transcriptome profiling of resistant and susceptible Cavendish banana roots following inoculati on with Fusarium oxysporum f. sp. cubense tropical race 4. BMC Genom. 2012, 13, 374.
  72. Zhu, Q.H.; Stephen, S.; Kazan, K.J.; In, G.; Fan, L.; Taylor, J.; Dennis, E.S.; Helliwell, C.A.; Wang, M.B. Characterization of the defense transcriptome responsive to Fusarium oxysporum-infection in Arabidopsis using RNA-seq. Gene 2013, 512, 259–266.
  73. Husaini, A.M.; Sakina, A.; Cambay, S.R. Host-Pathogen Interaction in Fusarium oxysporum infections: Where do we stand? Mol. Plant-Microbe Interact. 2018, 31, 889–898.
  74. Gwinn, K.D.; Hansen, Z.; Kelly, H.; Ownley, B.H. Diseases of Cannabis sativa caused by diverse Fusarium Species. Front. Agron. 2022, 3, 796062.
  75. AbuQamar, S.F.; Moustafa, K.; Tran, L.S. Mechanisms and strategies of plant defense against Botrytis cinerea. Crit. Rev. Biotechnol. 2017, 37, 262–274.
  76. Reboledo, G.; Agorio, A.; Vignale, L.; Batista-García, R.A.; Ponce De León, I. Botrytis cinerea transcriptome during the infection process of the Bryophyte Physcomitrium patens and angiosperms. J. Fungi 2021, 7, 11.
  77. Balthazar, C.; Cantin, G.; Novinscak, A.; Joly, D.L.; Filion, M. Expression of putative defense responses in Cannabis primed by Pseudomonas and/or Bacillus strains and infected by Botrytis cinerea. Front. Plant Sci. 2020, 11, 572112.
  78. Mersmann, S.; Bourdais, G.; Rietz, S.; Robatzek, S. Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol. 2010, 154, 391–400.
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