Chiang Mai Journal of Science

Occurrence and Seasonal Development of Plant Parasitic Algae Cephaleuros (Chlorophyta, Ulvophyceae) in Southern Thailand

1. INTRODUCTION

     The genus Cephaleuros (Kunze) E.M. Fries consists of green algae belonging to the family Trentepohliales in the division Chlorophyta. The algae in this genus are often referred to as “red rust” or “algal spots” and are frequently confused with fungal rust disease [1]. Algal spots typically occur on the upper leaf surfaces of host plants, although, in severe cases, they can affect both the upper and lower surfaces. In general, Cephaleuros species consists of filamentous cells that are aerial rather than aquatic, with erect structures such as sporangiophores and setae projecting perpendicularly from the algal thalli. Lesions on plants are often brightly colored due to carotenoid pigments, but can also be without discoloration, velvety, with several shapes. Cephaleuros depletes water and mineral nutrients from host tissues [2] and secretes harmful metabolites [3], causing necrosis of host tissues and thereby reducing the photosynthetic area [4].
     Studies on plant-parasitic Cephaleuros algae in Thailand have been limited over the past 10 years. An unidentified species has been referred to as Cephaleuors virescens, but without a clear identification key. However, according to a key to species of algae in genera Cephaleuros, Phycopeltis, and Stomatochroon [5], precise identification of parasitic algae was conducted in southern Thailand. For instance, Pitaloka [6] first described C. solutus on durian (Durio zibethinus) leaves based on morphological characters [5]. Later, ten species of Cephaleuros (C. diffusus, C. druetii, C. expansa, C. henningsii, C. lagerheimii, C. karstenii, C. parasiticus, C. pilosa, C. tumedae-setae, and C. virescens) were found to cause algal spot disease on several host plant taxa [7–14].
     Climate change can alter temperature, precipitation patterns, and atmospheric CO₂ levels [15]. It also impacts pathogen biology, host susceptibility, and interaction between plant hosts and pathogens, leading to the emergence of new diseases [15–17]. Recently, an increase in emerging diseases has been reported in southern Thailand, associated with sub-aerial algae [9,14] and plant pathogenic fungi [18,19]. However, detailed reports on the seasonal variation of plant-parasitic algae in the genus Cephaleuros in Thailand during the era of climate change are lacking. Therefore, this research investigated the seasonal development and frequency of algal thalli (lesions) on various host plants. The size and number of plant parasitic algae, as well as the production of reproductive cells, were periodically investigated on the leaves of several plants.

2. MATERIALS AND METHODS

2.1 Sample Collection and Morphological Identification
     Algal specimens were collected from three plant taxa (n = 20 per plant host per month), including longkong (Lansium domesticum), mango (Mangifera indica), and mangosteen (Garcinia mangostana) at the Pest Management field of Faculty of Natural Resources, Prince of Songkla University, Hatyai, Songkhla, Thailand (7°0’18’’N 100°29’58’’E) during summer (February–April) and rainy (May–January) seasons from 2020 to 2021. Algal thalli were removed from leaf samples with a razor blade. Macroscopic and microscopic features were observed using stereo and compound microscopes (Leica S8AP0, Leica DM750, Germany). Morphological characteristics (filamentous cells, setae, sporangiophores, sporangia, gametangia) were measured and recorded using a compound microscope (Leica DM750). Cephaleuros morphospecies were identified based on the key to species by Thompson and Wujek [5].

2.2 Seasonal Development Measurement of Plant Parasitic Algae
     Physical factors were compared with the number of algal lesions per leaf to clarify the seasonal variation of Cephaleuros species on three plant taxa. The key physical environmental factors, rainfall, humidity, and temperature, were acquired from the Center of Rubber Authority Thailand (RAT) in Hatyai, Songkhla, Thailand, throughout 2020–2021. The number of lesions on host plants and thallus sizes were measured on each leaf (n = 20). To clarify the development of reproductive structures, morphological characteristics were observed, and numbers of gametangia and sporangia were also recorded per random view of thalli on each leaf (n = 20).

2.3 Correlation between Physical Factors and Algae Development
     The physical factors, including humidity, rainfall, low temperature, and high temperature, were combined with biological factors, including thalli size, number of thalli, number of gametangia, and number of sporangia. The relationship between physical and biological factors was evaluated using Pearson correlation analysis. The correlation coefficient ranged from -1 to +1, whereas an absolute value of 1 represents a strong correlation.

2.4 Statistical Analysis
     Data on the numbers of thalli, gametangia, sporangia, and the size of thalli were subjected to analysis of variance (ANOVA) to assess differences between seasons. The data were analyzed using SPSS software version 15, and statistical significance was evaluated using Student’s t-test, where p<0.05 was considered a significant difference.

3. RESULTS

3.1 Physical Factors Measurements
     The relative humidity and temperature in southern Thailand were relatively stable, while rainfall accumulation fluctuated (Figure 1). The occurrence of plant parasitic algae was investigated in two seasons based on rainfall: summer (< 100 mm per month) and the rainy season (≥ 100 mm per month). Relative humidity at the study site ranged between 69.30–86.87 % in 2020, with summer ranging from 69.30–80.32 % and rainy season ranging from 76.65–86.87 %. In 2021, humidity ranged from 73.44–88.29 %, with summer ranging from 73.44–81.59 % and the rainy season ranging from 74.94–88.29 %. The air temperature was 23.60–33 °C during the summer and 23.40–31 °C during the rainy season in 2020. In 2021, the temperature ranged from 23.10–32.80 °C, in the summer, and 23.80–31.30 °C in the rainy season. The minimum rainfall was 0 mm (in summer), and the highest rainfall was 665.60 mm (in the rainy season) (Figure 1).

3.2 Occurrence of Plant Parasitic Algae
      Cephaleuros karstenii on L. domesticum, C. pilosa on G. mangostana, and C. virescens on M. indica, were previously identified based on morphology [9]. In this study, we compared morphological characteristics and seasonal development of these three Cephaleuros species on their respective host plant. The number and size of algal thalli were measured during both the rainy and summer seasons. The morphological characteristics differed between the summer and rainy seasons. Wilted and dry algal thalli were observed during the summer when rainfall was <100 mm in both observed years (2020–2021) (Figure 2a). Dry and distorted gametangia and sporangia, with no gametes or zoospores released, were also observed in this season (Figure 2a). However, when rainfall reached 100 mm in the rainy season, the number of fresh algal thalli increased in both years.

3.3 Seasons Influence the Size and Number of Plant Parasitic Algae
     The thallus size of each Cephaeluros species on the three plant hosts was compared between the summer and rainy seasons (Figure 2b and 2c). Thallus sizes of C. karstenii, C. pilosa, and C. virescens observed in the rainy season were 1.8±0.48, 1.8±0.67, and 3.8±1.13 mm, respectively, whereas those observed in summer were 2.1±0.28, 1.7±0.06, and 2.6±0.18 mm (Figure 2b). Average numbers of thalli of C. karstenii, C. pilosa, and C. virescens per leaf observed in the rainy season were 25.5±5.0, 15.6±2.8, and 32.2±2.5, respectively, significantly higher than those in the summer 5.2±3.0, 3.2±1.4, and 15.0±1.8 (Figure 2c).

3.4 Seasonal Development of Reproductive Structures
      Gametangia and sporangia of Cephaleuros in summer were dry, wilted, lacked orange pigment, and were without gamete or zoospore production. However, gametangia and sporangia on leaves during the rainy season were fresh orange in color. C. karstenii gametangia developed from July and released gametes from August to October 2020, and they were formed in June and released gametes from July to October 2021(Figure 3). Sporangiophores with sporangia formed in July and released zoospores from September to December 2020, and developed in June and released zoospores from July to November 2021 (Figure 3). For C. pilosa, gametangia developed in July and released gametes from September to November 2020. They developed in June and released gametes from July to September 2021. Sporangia developed on sporangiophores in July and released zoospores from September to December 2020, and in July and released zoospores from September to December 2021 (Figure 3). For C. virescens, gametangia developed in June and released gametes from August to October 2020, and they developed in May, releasing gametes from June to November 2021. Sporangia developed in July and released zoospores from September to December 2020, and in July and released zoospores from September to December 2021 (Figure 3).
     We also observed the seasonal impact on the development of gametangia and sporangia for each Cephaleuros species by investigating the numbers of gametangia and zoospores per random view of the thallus (Figure 4). The numbers of gametangia of C. karstenii, C. pilosa, and C. virescens observed in the rainy season were 97.5 ± 4.9, 125.2 ± 5.5, and 132.4 ± 9.7, respectively, which were significantly higher than in the summer: 13.2 ± 1.0, 15.5 ± 2.2, and 71.5 ± 2.1 (Figure 4a). The numbers of sporangia of C. karstenii, C. pilosa, and C. virescens observed in the rainy season were 209.4 ± 4.4, 254.2 ± 5.4, and 379.2 ± 9.2, respectively, significantly higher than the numbers in the summer: 68.5 ± 2.9, 66.3 ± 4.2, and 83.8 ± 8.1 (Figure 4b).

3.5 Relationships between Physical Factors and Algae Development
     Data were subjected to Pearson correlation analysis to test whether rainfall, humidity, low temperature, and high temperature influence algae development (thalli size, number of thalli, gametangia, and sporangia). There was no correlation among rainfall, thalli size, and number of sporangia of C. pilosa on G. mangostana, as the correlation coefficient was 0. Rainfall and humidity showed a negligible positive correlation with the number of thalli and number of gametangia of C. pilosa, as presented in blue (Figure 5). For the development of C. karstenii on L. domesticum, rainfall and humidity showed a positive correlation with the number of thalli, gametangia, and sporangia. However, there was no correlation between rainfall and thalli size (Figure 6). In the development of C. virescens on M. indica, rainfall showed a positive correlation with thalli size and the number of gametangia, while humidity showed a positive correlation with all growth parameters (Figure 7).

4. DISCUSSION

     Three plant species, L. domesticum, G. mangostana, and M. indica were found to host C. karstenii, C. pilosa, and C. virescens, respectively. The occurrence of algal thalli was restricted in the summer season in these three plant species, suggesting that suitable seasonal physical factors are crucial for algal development on the host plants. The infection of hosts, thalli development, and dispersal of gametes and zoospores of Cephaleuros have been reported to occur during the rainy season [2,20–22]. The number of algal thalli per leaf increased in the three plant species during the rainy season, which is consistent with observations by Salleh and Kamsare [22] and Muthukumar et al. [23].
     In this study, we found that the thallus sizes of C. karstenii on M. indica and C. pilosa on G. mangostana did not significantly differ between the summer and rainy seasons. However, the thallus size of C. virescens did differ between the two seasons. Pearson correlation analysis revealed a positive correlation between rainfall and thallus size for C. virescens on M. indica. This phenomenon may be due to the presence of active inocula (gametes and zoospores) and the ability of these inocula to penetrate the host plant [2,21,24,25]. Despite the positive correlation between rainfall and thallus size of C. virescens, the different host plant responses to algal infection may also play a role. Salleh and Kamsari [22] reported that Cephaleuros infection in Hevea brasiliensis increased with rainfall in Sungai Buluh, Malaysia. Our results also showed increased numbers of thalli per leaf, as well as increased gametangia and sporangia formation by the three Cephaleuros species during the rainy season.
     Mann and Hutchinson [21] found that infection by C. virescens of Camellia sinensis lasted from July to November, and zoosporangia formed the following April and May in Assam, India. Wolf [2] explained that infection by C. virescens in Magnolia grandiflora became evident during late September and early October, with gametangia and sporangia forming the following May in Florida, USA. Our study showed fresh thalli of the three Cephaleuros species developing on their respective host plants in June. Gametangia and sporangia began forming in June and July of 2020, respectively, and in June of 2021, during the rainy season with rainfall ≥ 100 mm in both observed years. This suggests that the period of greatest rainfall might be the key factor for Cephaleuros development and reproduction.
     Suématu [26] assessed the reproductive structures of C. virescens on several host plants, noting that gametangia developed and gametes were released in all seasons, while sporangia formed from May to November, and zoospores were released in July, in Wakayama, Japan. We found that gametangia developed in all seasons; however, fresh and active gametangia were observed during the rainy season, and gametes were released variably based on Cephaleuros species and host. All gametes were released during the rainy season. Since Thailand has tropical and subtropical regions that differ from the temperate zone in Japan, the development of reproductive structures and release of reproductive cells may be expected to differ. Muthukumar et al. [23] showed that zoosporangia of C. virescens were formed on plant leaves both during the rainy and summer seasons in India. In the present study, sporangia formed in all seasons, but fresh sporangia formed only in the rainy season. This is consistent with Marlatt and Cambell [27], who showed that the sporulation of Cephaleuros species infecting guava occurred during the rainy season (from July to September) in Florida, USA.

5. CONCLUSIONS

     Our results revealed the development of plant parasitic algae in the genus Cephaleuros on different hosts in southern Thailand. Correlation between physical factors showed that rainfall and humidity play a major role in thalli growth and reproductive structure development. This knowledge provides a better understanding of the seasonal development of plant parasitic algae, including the growth and progression of thalli, as well as the development of reproductive structures between the summer and rainy seasons. To our knowledge, no detailed report on the seasonal development of Cephaleuros species has been published in Thailand, making this study a significant contribution to filling that knowledge gap. Furthermore, this study suggests the need for an appropriate method to manage this plant parasite. However, there is no clear restriction of algal penetration and colonization in plant hosts, and the germination of gametes and zoospores in nature should be further investigated in future studies.

ACKNOWLEDGEMENTS

     This research was supported by the Center of Excellence in Agricultural and Natural Resources Biotechnology (CoE-ANRB) phase 3 and was partially supported by Thaksin University.

AUTHOR CONTRIBUTIONS

Prisana Wonglom: Conceptualization, Methodology, Resources, Validation, Writing - Original draft preparation. Narasinee Thithuan: Data curation, Software. Anurag Sunpapao: Visualization, Investigation, Supervision, Funding acquisition, Formal analysis, Project administration, Writing- Reviewing and Editing.

CONFLICT OF INTEREST STATEMENT

     The authors declare no conflicts of interest.

DECLARATION OF USE OF GENERATIVE AI

     During the preparation of this work, the author (s) used ChatGPT to perform language checking and formatting. After using this tool/service, the author(s) reviewed and edited the content as needed and took full responsibility for the content of the publication.

FUNDING

     The Prince of Songkla University and Thaksin University financially supported this research.

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