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Pantoea and Rice Plants
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This entry is adapted from the peer-reviewed paper 10.3390/agriculture11121278

Pantoea species are gram-negative bacteria from the Enterobacteriaceae family, generally associated with plants, either as epiphytes or as pathogens. In the last decade, Pantoea species are being regarded as re-emerging pathogens that are the causal agents of various diseases in rice plants. Inherently, they are also known to be opportunistic plant symbionts having the capacity to enhance systemic resistance and increase the yield of rice plants.

Pantoea rice microbiome symbiosis plant–microbe interactions

1. Classification and Biology of Pantoea Species

The Pantoea species are generally recognized as non-encapsulated, non-spore-forming gram-negative bacteria from the Enterobacteriaceae family [1]. Before 1989, pathogenic bacteria from this order belonged to a single genus known as Erwinia. The genus Pantoea was proposed based on differential sequence in the DNA hybridization group separating them from Erwinia [2]. Currently, there are 25 described species and two subspecies that belong to this genus that have been isolated from various environments such as water, soil, human, animals, and plants [3][4][1].
Most species in the Pantoea genus are observed to have yellowish pigment, gram-negative cell wall, rod-shaped, peritrichous flagella and possess facultative anaerobic metabolism [5][6][7][8]. They show negative reactions towards oxidation, arginine dihydrolase, citrate utilization, sorbitol fermentation and nitrate test. On the other hand, these species are positive for catalase, gelatine and starch hydrolysis tests [9][10][11]. Bacteria from this genus are also capable of exhibiting acid production from various carbon sources such as maltose, trehalose, palatinose and L-arabinose [12].
Pantoea species can grow in a wide range of pH from 2 to 8, with optimum growth occurring at pH 7. The optimum growth temperature was at a range of 28 °C to 30 °C and the bacteria had been documented to tolerate a wide range of temperatures, from 4 °C to 41 °C. Additionally, optimal growth rate may be achieved when NaCl concentration is between 100–300 mM [10][13].
Multilocus Sequence Analysis (MLSA) using marker genes such as 23S rRNA, rpoB, gyrB, and dnaK are often used for the exploration of the sequence discontinuities among the Pantoea species [1]. Sequence variations within housekeeping genes such as leuS, fusA, gyrB, rpoB, rlpB, infB, and atpD have also been used routinely to refine interspecific phylogenetic positions of species from the genus Pantoea [1][14].
Another strategy to resolve identification of Pantoea specimens is the use of a mass spectrometry-based approach, namely the matrix-assisted laser desorption ionization-time of flight (MALDI-TOF). Unfortunately, it has been reported that 24% of Pantoea species had been misidentified using this approach [15], which appears to suggest that a multiple gene sequencing strategy or whole genome-based identification methods are more reliable and accurate for Pantoea identification.

2. Beneficial Impacts of Pantoea-Rice Plant Interactions

Generally, the existence of symbiotic relationships between plants and microbes is nothing new and has been well documented [16]. Although initially symbiotic microorganisms were considered to be neutral regarding their effects on host plants, recent evidence that points towards their positive impact on plant growth and development has been verified in a broad range of crops [17]. Direct plant growth promotion by microbes is based on improved nutrient acquisition, hormonal stimulation and alteration of physiological and genetic make-up. Indirectly, they may also reduce microbial populations that are harmful to the plant, acting as agents of biological control through competition, antibiosis, or systemic resistance induction [18].
Various studies on the Pantoea species have indeed shown that they possess many beneficial traits that could be used in rice farming systems such as combating rice plant pathogens and promoting growth and fitness [19]. As a matter of fact, members of the genus Pantoea are frequently detected around rice rhizosphere [20], on rice phyllosphere [21], inside rice plant tissues [22][23][24], and on rice seeds [25]. These enormous potentials serve only to suggest that perhaps it would be possible to develop Pantoea inoculants for use in sustainable rice production in the future.

2.1. Impacts on Rice Plant Growth and Yield

Reports from more than a decade ago have suggested that the inoculation of Pantoea to rice plants promoted rice plant development and yield. Zhang et al. [26] reported that the application of P. agglomerans to rice plants could enhance several growth parameters such as leaf growth, root elongation, root hair growth and stem growth. Furthermore, under the agroecosystem of southern Spain, Megías et al. [20][27] revealed that P. ananatis when applied to rice plants showed plant growth-promoting attributes, including the capacity to synthesize siderophores, cellulose, indole acetic acid (IAA) and 14 different molecules of N-acyl-homoserine-lactones (HSLs). Subsequently, inoculation of rice plants with P. ananatis significantly increased plant growth and crop yield by 60%, indicating a high potential for its use as a commercial inoculant. More recently, a study by Sun et al. [19] showed that inoculation of P. alhagi in rice plants increased fresh weight, root length, and shoot length of rice plants compared with control plants.

2.2. Impacts on Rice Plant Physiology

In addition to increased growth and yield, rice plant physiology can also be improved in the presence of Pantoea species. When P. agglomerans was applied, the P content in rice plants was significantly increased in comparison to control plants [28]. Also, inoculation of rice plants with P. agglomerans significantly enhanced the transportation of the photosynthetic assimilation product from the source (flag leaves) to the sink (stachys) when compared to control plants [23]. This result indicated a superior metabolism capacity inside the plant cells following the exposure to Pantoea. Furthermore, Sun et al. [29][19] reported that colonization of rice roots by P. alhagi recorded a 26.3% increase in chlorophyll content, as well as up-regulated expression of proline synthase, a down-regulated expression of proline dehydrogenase, and enhanced antioxidant enzyme activities compared with uninoculated plants.

2.3. Alleviation of Biotic Stress

Association of rice plants with different strains of Pantoea improved their ability to withstand biotic stress. For example, P. ananatis had been shown to be antagonistic to the plant pathogen Xanthomonas spp., resulting in an improved rice plant survival [20][27]. In another example, P. ananatis showed a significant biological control efficacy (more than 50%) towards rice blast caused by Magnaporthe grisea in greenhouse and field experiments. This evident decrease in the M. grisea severity in greenhouse and field experiments was attributed to the ability of P. ananatis to secreting extracellular hydrolytic enzymes [30]. Similarly, when rice plant roots were pre-treated with P. agglomerans prior to infection by fungal pathogen M. oryzae, the number of blast lesions in rice caused by M. oryzae was reduced. Further characterisation showed that the defence response elicited in rice by P. agglomerans is mediated through jasmonic acid and ethylene signalling pathways [31].

2.4. Induction of Abiotic Stress Tolerance

Root colonization by the Pantoea species induces systemic abiotic tolerance in plants. Early studies by Zeng et al. [32] indicated that P. agglomerans could stimulate the growth of rice plants under poor soil conditions. In their report, it was noted that rice plants associated with P. agglomerans grew much better compared to uninoculated control plants in low-nutrient soils. Later, Bhise and Dandge [33] reported a significant improvement in plant growth supplemented with P. agglomerans inoculum in terms of increased length, biomass, photosynthetic pigment, and decreased level of proline and malondialdehyde under salt stress conditions. Inoculated plants also exhibited decreased sodium and increased calcium and potassium uptake. In a related study, Sun et al. [29] revealed that colonization of rice plants by P. alhagi increased salt resistance of rice through increasing the K+/Na+ ratio, antioxidant enzyme activities and proline content, and decreasing malondialdehyde content. Moreover P. ananatis ameliorated the oxidative stress in rice induced by NaCl and Na2CO3 treatment. The malondialdehyde content and various antioxidant enzyme activities decreased upon P. ananatis inoculation in salt-affected rice plants [34]. Recently, Ghosh et al. [35] reported the ability of P. dispersa in enhancing rice seedling growth with a simultaneous reduction in arsenic uptake, and ethylene levels in plants.
Another report by Sun et al. [19] revealed that foliar spray of exopolysaccharide (EPS) that had been derived from P. alhagi to rice plants was able to increase drought resistance of rice. Further analysis showed that malondialdehyde content in rice tissue was reduced while total chlorophyll, proline and soluble sugar content were enhanced. The researchers also noted that the activity of antioxidant enzymes- superoxide dismutase, peroxidase, and catalase, also significantly increased.
All of the studies discussed above indicated that Pantoea species could be used as effective biocontrol agents for various rice diseases. Previous studies also highlighted the capacity of Pantoea species in improving rice plant’s tolerance towards abiotic stress, thereby contributing to better plant growth and yield. The efficacy of applying Pantoea inoculants in rice production has become more evident every year. However, more studies on the understanding of the capability of Pantoea species in enhancing rice plant development and the mechanisms involved are needed for acquiring maximum benefits from their application.

3. Detrimental Impacts of Pantoea-Rice Plant Interactions Leading to Rice Diseases

As mentioned previously, despite displaying beneficial roles in association with their host plants, Pantoea species had recently been regarded as a re-emerging pathogen based on the increasing number of reports of their involvement in diseases occurring in rice plants worldwide. Of the twenty-five known species that belong to the genus of Pantoea, some species have been reported as associated with rice diseases and they include P. dispersa, P. agglomerans, P. stewartii, P. wallisii and P. ananatis [36]. As early as 1983, a study by Azegami [37] indicated that the palea browning disease of rice in Japan was caused by Erwinia herbicola (E. herbicola was later known as P. agglomerans). A few years later, in 1986, Kim et al. [38] reported another case of brown discoloration of inner palea of rice occurring at the experimental field of Chonnam Provincial Rural Development Administration, Korea. The pathogenic bacterium was again identified as E. herbicola. According to an early observation by Tabei et al. [39], E. herbicola entered the lemmata and paleae through the stomata and multiplied in the intercellular space of the parenchyma. Stomata are mainly open on the inner surface of lemmata and paleae, a few on the outer surface of lemmata, and connected through the intercellular space of parenchyma.
In 2002, P. ananatis was described for the first time as the causative agent of stem necrosis disease in rice. The symptoms were characterized by necrotic lesions on the rachis and stem, extending into the flag leaf sheath and stopping at the second node. Another symptom observed was a fine ‘mottling’ of brown and green tissue above and below the top node, which subsequently affected the grain quality [40].
Pantoea species can also cause rice seeds to lose their viability as reported by Brazilian researchers. The pathogens were isolated from seed embryos by aseptically removing the seed coat and the bacterium was subsequently identified as P. agglomerans. It was also found that seeds associated with P. agglomerans when grown in a greenhouse for multiplication purposes showed poor or no germination [41]. Another report in China revealed that P. ananatis was able to cause severe discoloration of rice grains. Initially, at early flowering stage, some water-soaked lesions appeared on the lemma or palea, which would then turn brown in infected plants. These resulted in immature and lighter grains on panicles at harvest stage [42]. Grain discoloration disease associated with P. ananatis was also detected in Primorsky Krai, Russia. During the harvest season, bacterial yellow ooze was observed on panicles of infected rice plants, and the harvested grains were mostly immature and empty [10].
A more recent observation made in various rice cultivation systems in Asia, America, Africa and Europe was that the association of Pantoea species and rice plants can cause severe leaf blight disease infections (Figure 1). Field survey conducted in Benin and Togo reported that the P. ananatis and P. stewartii-infected rice leaves showed orange-brown lesions on one or both halves of the leaf blade [43][44]. Another report from a Russian rice field indicated a water-soaked symptom that led to the brown coloration appearing on plants’ lemma and resemble a typical leaf blight symptom caused by P. ananatis [10]. Rice plants in Venezuela which were colonized by P. agglomerans also showed leaf blight symptoms. The rice leaves appeared as yellow or brownish lesions and later become dry, illustrative of cell death [12].
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Figure 1. Leaf blight disease caused by Pantoea species in Selangor, Malaysia; (a) Highly infected rice field with a yellowish lesion on the leaves, (b) Close-up view of the infected leaf with a lesion at the edge, (c) Comparison between healthy leaf and leaf infected with the Pantoea species (Photos courtesy of Muhammad Nazri Ishak).
In the period of November–December 2017 of the second season of rice planting in Malaysia, several rice plots showed water-soaked lesions at the tip of the leaf and became brownish lines along the leaf margin. The causative pathogen was subsequently identified as P. stewartii [11]. Similar symptoms had also been detected in another local case at Selangor, Malaysia in 2016. The rice plants showed brownish lines along the leaf margins and eventually the entire leaf became dry [45]. Due to the reduction of the leaf area, the photosynthesis rate is affected, and this inadvertently led to reduced yield and quality of the rice grains. Arayaskul et al. [46] recently reported the first incidence of leaf blight associated with P. ananatis and P. stewartii in Thailand. The symptoms reported were similar to those made by other countries i.e., yellowish, light brown, to slightly reddish spots on leaves. Reports from various countries describing the rice diseases associated with Pantoea species are summarized in Table 1.
Table 1. Pantoea species associated with rice diseases.
Table
Countries Causative Agents Symptoms Rice Diseases References
Malaysia P. wallisii Water-soaked lesions at the tip of the leaf and turning into brownish lines along the leaf margin Leaf blight [36]
China and Russia P. ananatis Light, rusty, water-soaked lesions appearing on the lemma or palea and then turned brown Grain discoloration [10][42]
Malaysia, Turkey, Korea, and Venezuela P. agglomerans Water-soaked stripes or light brown-to-slightly reddish spots on the upper blades of the leaves Leaf blight [36][7][9][12]
Japan, Korea, and China P. agglomerans Brown discoloration of inner glume (palea) Palea browning disease [37][38][47]
Korea P. ananatis Necrotic spot and brown discoloration on glumes and stems of rice Sheath rot [48]
Italy P. ananatis Light brown lesions, which, over time, darkened, coalesced and enlarged resulting in the uniform browning of the palea Palea browning [49]
India, Benin, Malaysia, Thailand, and Togo P. stewartii Yellowing symptoms or one to two orange or brown stripes on one or both halves of the leaf blade Leaf blight [11][43][44][46][50]
India, Russia, Benin, Togo, China, Turkey, Thailand, and Malaysia P. ananatis Water-soaked stripes with yellowing color, which later turned into brown stripes on the upper part of leaves Leaf blight [6][8][10][43][44][45][46][51][52]
Australia P. ananatis Necrotic lesions occurring on the rachis and stem, extending into the flag leaf sheath and stopping at the second node Stem necrosis [40]
Brazil P. agglomerans Little or slow germination of seed Seed dormancy [41]
Malaysia P. dispersa Brownish stripes, which subsequently turn pale and dry on leaf blades Leaf blight [45]

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