Bioprospecting Desert Plants: History
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Subjects: Agriculture, Dairy & Animal Science
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Qiuwei Zhang

In deserts, endophytic microbes help plants thrive in dry, nutrient-poor soils by increasing nitrogen and phosphorus availability and alleviating stress caused by heat, inadequate moisture, and pathogen attack. These desert endophytes can be isolated from their hosts and then placed into non-native hosts, such as crop plants, in order to confer similar benefits to their new hosts. Screening desert plants for beneficial endophytes allows for the discovery of new biofertilizers and biocontrol agents that may be especially helpful in arid regions or farmland areas experiencing increasing  drought frequency due to climate change. 

  • endophytes
  • biostimulant microbes
  • plant–microbe interactions
  • climate change
  • desert plants

1. Introduction

Deserts present unique challenges for plant growth and survival. Infrequent and unpredictable precipitation, combined with high rates of evapotranspiration, results in dry surface soils with high salt concentrations [1]. In addition to being salty, desert soils are often nutrient poor, lacking in biologically accessible nitrogen and phosphorus [2][3]. The formation of “desert pavements” on top of desert soils reduces water penetration [4] and deters plant growth [5]. Air temperatures in deserts can fluctuate dramatically, sometimes by as much as 38 °C in the span of a day [6]. Overall, deserts are hostile environments for most plants, yet certain plant families have evolved to survive in deserts.

In addition to physical adaptations (such as CAM photosynthesis and modified leaf structures) that allow them to thrive in dry, nutrient-poor soils, desert plants also take advantage of microbial endophytes. Endophytes are defined as microbes that colonize plant tissues without causing apparent harm to their hosts [7]. They can be found in all land plants and are often required to maintain the health of their plant hosts [8]. Some endophytes are culturable in vitro, but many cannot be cultured outside of their specific host tissues [9][10]. Endophytes that can be cultured in vitro can be transferred from their source host into a compatible secondary host to provide similar benefits [11][12]. The agriculture industry in particular uses endophyte inoculants for commercial purposes as biostimulants and biocontrol agents [13][14][15][16]. However, despite the commercial and scientific interest in endophytes, not much research has been performed on the endophytes of wild plants, and even less research has been performed on the endophytes of wild desert plants.

Desert plants may serve as an untapped source of novel endophytes for use in agriculture, especially in arid farming areas where water and soil nutrients are at a premium. Desert endophytes may also have applications worldwide, as global climate changes increasingly subject croplands to abiotic stressors common in deserts. Rising carbon dioxide levels are expected to result in longer and more severe instances of drought, including instances of agricultural drought, which is characterized by decreases in soil moisture that negatively affect crop growth [17][18][19]. Likewise, instances of abnormally heavy rains and flooding are also expected to increase [20][21]. In addition, calls for reduced applications of chemical fertilizers, which are known to contaminate water sources by means of leaching and runoff [22][23][24], will lead to reduced soil nutrient levels that will require more efficient uptake by crops. The application of desert plant endophytes to crops may serve to alleviate some of the problems that the agricultural industry must contend with, both currently and in the future, though special care should be given to ensure that these endophytes will synergize with the new hosts’ native microbiomes. A switch from agrochemicals to microbe-based alternatives would also have the added benefit of public support, as evidenced by the increasing consumer demand for organic-certified foods [25][26][27] and the increasingly negative perceptions of chemical pesticides [28][29][30].

2. Microbial Endophytes Present in Desert Plants

Identification of the most common genera may help guide researchers who are interested in bioprospecting desert plants for beneficial endophytes. However, it is important to note that the genera mentioned below are composed only of culturable endophytes. There may be many more genera that are common to desert plant microbiomes but are unculturable outside their native host tissue; therefore, they are omitted, as unculturable microbes are of little commercial use as biostimulants and biocontrol agents despite their potential benefits. In addition, it must be mentioned that the diversity of culturable endophytes may not reflect the true diversity of culturable endophytes due to the lack of research on the topic.

A meta-analysis of 12 studies [31][32][33][34][35][36][37][38][39][40][41][42] aimed at identifying culturable bacterial endophytes of various desert plants revealed that all isolates belonged to one of four major phyla: Proteobacteria, Firmicutes, Actinobacteria, and Bacteroidetes. Out of a total of 717 bacterial isolates identified, 47.14% belonged to the phylum Proteobacteria, 26.22% belonged to the phylum Firmicutes, 22.55% belonged to the phylum Actinobacteria and 2.09% belonged to the phylum Bacteroides [43]. Of these four phyla, certain genera appear to be much more common than others. The most common Proteobacteria is Pseudomonas, comprising of 15.68% of all Proteobacteria isolates, but other genera, such as Acinetobacter and Gluconobacter, also appear at similar frequencies. The most common Firmicutes is Bacillus, comprising of 78.72% of all Firmicutes isolates. The most common Actinobacteria is Microbacterium, comprising of 51.70% of all Actinobacteria isolates. The very limited number of culturable isolates belonging to phylum Bacteroides makes it difficult to estimate what the most common genus is.

A meta-analysis of 7 studies [44][45][46][47][48][49][50] aimed at identifying culturable fungal endophytes of various desert plants revealed that 88.73% of the isolates belonged to the phylum Ascomycetes, 9.68% were sterile forms, 0.83% belonged to the phylum Zygomycota, and 0.75% belonged to the phylum Basidiomycota [43]. A majority of ascomycete endophytes are members of the Pezizomycotina, with a few belonging to the Saccharomycotina and 5 with uncertain taxonomy. All of the Basidiomycete endophytes are members of the Agaricomycotina and Pucciniomycotina. All of the Zygomycete endophytes are members of the Mucoromycotina. Delving down to the genus level, certain genera appear to dominate each class of fungi. The most common Dothideomycetes are Alternaria and Phoma are the most common genera, comprising of 30.75% and 28.68% of all Dothideomycetes isolates, respectively. The most common Sordariomycete is Fusarium, comprising 27.01% of all Sordariomycetes isolates. The most common Eurotiomycete is Penicillium comprising 71.28% of all Eurotiomycetes isolates. Due to the small number of isolates obtained for the other classes of fungi, it is unknown if any dominant genera exist.

It is possible that the ability of desert endophytes to confer benefits to their hosts is not determined by their taxonomy, but rather by the expression of certain genes related to biotic and abiotic stress resistance. Further studies on the transcriptomes and metabolomes of desert endophytes would help tease out important genes that are common between beneficial desert endophytes.

3. Effects on Nutrient Acquisition

Plants require a variety of nutrients to support their growth and development, the most important of which are nitrogen and phosphorus. Nitrogen and phosphorus are considered to be limiting factors for crop growth, hence why nitrogen and phosphorus fertilizers are commonly used in agriculture. However, heavy usage and reliance on these fertilizers has resulted in nonpoint pollution of surface waters via leaching and runoff [51][52], which damages aquatic ecosystems [52][53][54] and present dangers to humans who rely on or come into contact with contaminated waters [52][55][56]. In order to reduce the impact of agriculture on the surrounding ecosystems, researchers have been trying to find environmentally friendly alternatives for supplying nitrogen and phosphorus to crops. One area of focus has been on endophytic microbes, which may be able to reduce a crop’s external nitrogen and phosphorus needs. Desert soils are naturally deficient in nitrogen and phosphorus, which may select for endophytes that allow their hosts to use available nutrients more efficiently or acquire them from novel sources.

Many species and strains of the most commonly found desert plant bacterial endophytes (Proteobacteria, Actinobacteria and Firmicutes) have the capability to be nitrogen fixers [57]. The nitrogen-fixing ability of the most common genus of bacterial endophytes, Bacillus, has been well documented amongst certain species, namely B. polymyxa, B. macerans, and B. azotofixans [58][59][60]. The second most common genus of bacterial endophytes, Pseudomonas, has also been shown to have nitrogen-fixing members, namely P. stutzeri [61][62][63]. Less common endophytes, such as Klebsiella [64] and Pantoea [65] may possess nitrogen-fixing capabilities as well. Indeed, diazotrophic Bacillus, Pseudomonas, and Klebsiella, as well as Acinetobacter, Cronobacter, Enterobacter, Enterococcus and Leuconostoc, have been found in Agave tequiliana [37]. However, the most interesting and potentially beneficial diazotrophic endophytes are likely to be found in pioneer plants that colonize disturbed areas, particular areas with low amounts of soil.

Phosphate-mobilizing microbes have also been found within plants as endophytes. Generally, phosphate-solubilizing bacterial endophytes belong to the Firmicutes or Proteobacteria phyla; examples include Pseudomonas [66], Burkholderia and Rahnella [67], Bacillus [68][69], and Enterobacter and Pantoea [69]. Most phosphate-solubilizing fungal endophytes are ascomycetes, though some may be basidiomycetes. Examples of ascomycete phosphate solubilizers include Penicillium [70][71], Trichoderma [72], Aspergillus , and Fusarium and Humicola [73]. An example of a basidiomycete phosphate solubilizer is Piriformospora [71]. All of the above genera, with the exception of Humicola, have been found as endophytic microbes in desert plants [43].

Nitrogen-fixing and phosphate-solubilizing endophytes may be especially abundant in pioneer plants.  Research performed on the roots of two pioneer plants – the cardon cactus Pachycereus pringlei and the cactus Mammillaria fraileana – revealed strains of endophytic bacteria that were able to fix nitrogen, even though the roots themselves contained no nodules [36][40][65][74]. The cacti used in these studies grow in areas where very little, if any, soil is present, so it is unlikely that they are relying on soil nitrates to fulfill their nitrogen needs, suggesting that the two cacti obtain their nitrogen from other sources, likely their diazotrophic endophytes. In addition, these two cacti also had endophytic bacteria that could weather rocks and solubilize inroganic phosphates.

4. Effects on Abiotic Stress Resistance

Due to climate change agricultural regions are experiencing greater and greater frequencies of drought [18]. Plants growing under drought conditions must contend with a combination of water stress, heat stress, and salt stress, all of which negatively impact crop productivity and yields. These effects are compounded by water scarcity, especially in areas where water usage is mismanaged or where water sources are overexploited [75][76]. The ballooning global population will only accelerate the increases in demand and decreases in supply of freshwater [77] and force nations to plant and grow crops to in suboptimal conditions to meet food demands [78][79][80]. The development of crop adaption mechanisms against drought stress and heat stress will become ever more important as time goes on. Currently, the agricultural industry develops and utilizes drought-resistant cultivars to reduce the impacts of drought on yields, but the introduction of drought- and heat-resistant microbiomes into crops could also be considered as a supplement to breeding for resistance.

The available research on endophyte-based alleviation of drought and heat stress has shown that both bacterial and fungal endophytes have the ability to induce drought and heat resistance in crop hosts. Eke et al. [35] transferred endophytic bacteria from the cactus Euphorbia trigonas Mill to tomatoes, resulting in improved plantlet response to water stress. Zahra, Hamedi & Mahdigholi [81] inoculated sunflowers with Streptomyces spp. isolated from Pteropyrum olivieri, which increased seedling tolerance to drought stress.

Some research shows that desert endophytes, particularly bacterial endophytes, were able to improve host response to salt stress when inoculated into glycophytes. Trials on Arabidopsis thaliana showed that inoculation with Bacillus [39], Enterobacter [82], and Athrobacter, Pantoea, and Microbacterium [32] isolates from various desert plants showed improved resistance to salt stress and improved growth compared to non-inoculated controls. Bacillus spp. were shown to alleviate salt stress in tomatoes as well [83]. In addition, Streptomyces spp. isolated from Pteropyrum olivieri increased sunflower seedling tolerance to salt stress [81]. Bacillus, Enterobacter, Pantoea, Microbacterium and Streptomyces are all common bacterial endophytes of desert plants [43], suggesting that more salt-resistance-conferring bacterial endophytes are yet to be discovered. In terms of fungi, a cross-taxonomic group of fungi referred to as dark septate endophytes have been shown to alleviate the symptoms of salt stress in glycophytes as well [84]. However, it is important to note that only some of the above endophytes are able to promote host growth in normal conditions [85][81], while others are only able to promote host growth in saline environments [41][85][84].

5. Effects on Biotic Stress Resistance

While deserts are generally known for their abiotic stressors, biotic stressors are still present. Pathogens such as Texas root rot (Phymatotrichopsis omnivora) and pests such as desert locusts exert selection pressure on native desert plants to acquire sources of resistance, such as endophytes, against their antagonists. Learning more about the endophytic microbiome of desert plants may allow researchers to find beneficial endophytes that can be used to adapt crops to biotic stressors unique to desert habitats, and perhaps to biotic stressors outside of deserts.

The lack of water and nutrients in desert soils likely encourages symbiotic interactions between plants and microbes, particularly in the rhizosphere and root endophytic compartments. However, desert plants are still subject to pathogen attacks, even if such instances of such attacks may not be well documented in the wild. For instance, Texas root rot is a fungal pathogen that inhabits the alkaline desert soils of the southwestern United States and northern Mexico which can attack a variety of plants, mainly dicots [86]. Native desert dicots such as prickly pear cacti, desert willow, and palo verde are notably tolerant of the disease, perhaps partially due to the presence of their endophytes. Such disease pressure is likely present in other desert environments and researching the disease resistance capabilities of desert plants may produce novel solutions for growing non-native crops in desert environments that contain potent pathogens.

Several instances of desert endophytes conferring resistance to fungal pathogens have already been reported. Endophytic P. indica from the Thar Desert increased barley resistance to root pathogens [87], while Bacillus and Enterobacter from Thymus vulgarius in Egyptian deserts increased tomato resistance to Fusarium oxysporum [83].

According to the resource availability hypothesis (RAH), plants with low growth rates due to poor resource availability invest more into anti-herbivory defenses [88]. Deserts are some of the most resource-poor environments on Earth and contain some of the slowest growing plants on the planet, so desert plants should have many defenses against herbivores in accordance with the RAH. However, some suspect that broad-host-range endophytes, like those found in desert plants, may encourage herbivory in order to transmit spores and hyphae to new hosts [89][90][91]. If it is found that desert endophytes, or at least a subset of them, can deter herbivory while still able to colonize a large variety of plants, it may be worthwhile to introduce desert endophytes into crop plants to alleviate yield losses from insect damage.

There is evidence to suggest that plant resistance to insect damage is increased by the presence of both bacterial [92] and fungal [93][94] endophytes. Some studies on fungal desert endophytes demonstrate that they are able to increase host resistance and tolerance to herbivory: P. indica from the Thar Desert increases plant tolerance to root herbivory [95] and an Epichloë endophyte from a grass from the Sonoran Desert reduces seed harvesting by leaf cutter ants [96]. Unfortunately, there appears to be no studies regarding bacterial desert endophytes and their effect on herbivory.

This entry is adapted from the peer-reviewed paper 10.3390/biology10100961

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