Molecular defense responses in roots and the rhizosphere against Fusarium oxysporum

Abstract

Plants face many different concurrent and consecutive abiotic and biotic stresses during their lifetime. Roots can be infected by numerous pathogens and parasitic organisms. Unlike foliar pathogens, root pathogens have not been explored enough to fully understand root-pathogen interactions and the underlying mechanism of defense and resistance. PR gene expression, structural responses, secondary metabolite and root exudate production, as well as the recruitment of plant defense–assisting “soldier” rhizosphere microbes all assist in root defense against pathogens and herbivores. With new high-throughput molecular tools becoming available and more affordable, now is the opportune time to take a deep look below the ground. In this addendum, we focus on soil-borne Fusarium oxysporum as a pathogen and the options plants have to defend themselves against these hard-to-control pathogens.

Abbreviations

ET

ethylene

ISR

induced systemic resistance

JA

jasmonic acid

PR

pathogenesis-related

ROS

reactive oxygen species

SA

salicylic acid

Biotic stresses in the roots and rhizophere include plant disease-causing pathogens, such as fungi, oomycetes, bacteria and viruses, as well as insects, nematodes, other herbivores and parasitic plant interactions. Fungal pathogens can be simply classified into 2 categories, biotrophic or necrotrophic, depending on how they acquire nutrients from the host plant. Many biotrophs live in the intercellular region between mesophyl cells, and some produce haustoria as a feeding structure which allows them to absorb nutrients from the host plant while evading recognition or defense responses.^1,2 Salicylic acid (SA)-, reactive oxygen species (ROS)- and localized programmed cell death, known as the hypersensitive response, provide an effective mechanism to isolate infection with obligate biotrophic pathogens.³ In contrast, necrotrophic pathogens produce enzymes to degrade cells and often toxins to kill host tissues to absorb nutrients.⁴ Plants are able to effectively defend against these pathogens via the jasmonic acid (JA) and ethylene (ET) pathways that produce pathogenesis-related (PR)-proteins and secondary metabolites while suppressing ROS production (Fig. 1). However, it is important to note that some pathogens may behave as both a necrotroph and a biotroph depending on the different stage of the infection cycle. These hemi-biotrophic pathogens typically act as biotrophs at an early stage, feeding on living cells and establishing infection before shifting to a necrotrophic phase to complete their life cycle.⁵

Figure 1.

Plant defense pathways against pathogens are linked to interactions with beneficial rhizosphere microbes. Plants use different defense responses to deal with different types of pathogens. For successful defense against biotrophic pathogens, plants typically activate the salicylic acid (SA) pathway and produce reactive oxygen species. This can lead to a localized hypersensitive response and programmed cell death to isolate the pathogens but also systemic acquired resistance against subsequent infections in other parts of the plant. On the other hand, the JA and ET pathways antagonize the SA pathway by preventing programmed cell death and are typically activated to deal with necrotrophic pathogens and some insects. In addition the JA/ET pathway is involved in interaction with beneficial rhizosphere microbes that provide benefits by priming the plant to respond faster and stronger to subsequent infections (induced systemic resistance).

Fusarium oxysporum is a hemi-biotrophic root pathogen that infects a number of plants, including cotton, tomato, banana and Arabidopsis.⁶ F. oxysporum is believed to be able to manipulate defense pathways, and previous research has identified that some Arabidopsis-infecting isolates hijack the JA pathway,^7,8 a pathway typically used for induced systemic resistance (ISR) by beneficial rhizophere microbes or against necrotrophic pathogens or insects. Impaired JA-signaling mutants, myc2, coi1 and pft1/med25, although more susceptible to other pathogens, showed strong resistance against F. oxysporum.^7,9,10 coi1-mediated F. oxysporum resistance was independent of both JA- and SA- dependent defense gene expression, but correlated with compromised non-defensive aspects of JA-dependent responses in this mutant, suggesting that F. oxysporum hijacks non-defensive aspects of the JA-signaling pathway to enhance disease. Pantelides et al. (2013) also suggested that F. oxysproum hijacks ETR1-mediated ET signaling to promote disease development in Arabidopsis.¹¹ ETR1 is an ET receptor and acts upstream of the ET pathway regulator CTR1.¹² ET and JA work tightly together to confer resistance against necrotrophic pathogens.¹³

However, many F. oxysporum strains live in the soil and often colonize roots as endophytes without causing damage or even provide benefits against pathogens.¹⁴ A wealth of literature has reported that Fusarium wilt can be controlled by non-pathogenic strains of F. oxysporum in numerous crops, such as banana, asparagus, basil, chickpea, watermelon, cyclamen, tomato, spinach, cucumber, and melon (for a comprehensive review see¹⁵). Although there are a few reports that these protective F. oxysporum strains were effective against other pathogens including Meloidogyne incognita, Phytophtora capsici, and Pythium ultimum, they generally exhibit biological control attributes against pathogenic F. oxysporum.^16-18 However, other well-known biocontrol agents against F. oxysporum, including Trichoderma and Pseudomonas, inhibit a wider range of pathogens.¹⁵ Recent studies have shown that plants are able to recruit certain microbes in their rhizosphere during defense signaling.¹⁹ These “soldier” microbes are known to produce antimicrobial and insecticidal compounds and differ from those under normal growth condition where most beneficial microbes assist with nutrient supply and plant growth promotion. It would interesting to study whether protective F. oxysporum strains can be actively recruited during plant defense signaling.

Apart from using biological control agents, genetic manipulation to increase resistance to F. oxysporum has made progress on several fronts. It was already mentioned above that desensitizing plants for JA signaling provided resistance in Arabidopsis. McGrath et al. (2005) identified a transcription factor-encoding gene, ERF4, which is a negative defense gene regulator controlled by JA and fungal pathogens.²⁰ Inactivation of ERF4 showed an increase resistance to F. oxysporum. Recently, Chen et al. (2014) reported that erf72 Arabidopsis mutants showed increased resistance to F. oxysporum.²¹ ERF72 has a role in ROS response,^22,23 but erf72 plants did not show a noticeable altered oxidative burst in the root region. Chen et al. (2014) also examined the pub22/23/24 U-box type E3 ubiqutin ligase triple mutant, which is known to possess enhanced ROS production in response to pathogen challenge.²¹ However pub 22/23/24 mutants showed increased resistance to F. oxysporum, suggesting that ROS homeostasis and heightened innate immune responses provide protection against soil-borne F. oxysporum.

Conclusions

Although soil-borne diseases result in significant yield losses world-wide, relatively little is known how plants are able to defend themselves against these pathogens. Root-specific defense gene expression, structural responses, secondary metabolite and root exudate production in the rhizosphere may all assist in fighting off soil-borne pathogens and pests, and perhaps also promote colonization of plant defense–assisting beneficial microbes. Soil-born F. oxysporum appears to be an “accidental” pathogen that disguises as a beneficial microbe to activate the JA pathway to gain entry into the cell as a hemibiotrophic pathogen. Further studies of the early steps leading to F. oxysporum colonization of root cells are needed to elucidate the underlying mechanisms of recognition and early signaling during this interesting plant-microbe interaction.

Disclosure of Potential Conflicts of Interest

No potential conflicts of interest were disclosed.