ABSTRACT
Mycorrhiza is a symbiotic mutualism among the plant roots with fungi. Its known as biofertilizer. The research aims to describe the development of mychorrizal research during the period of 1980 to 2020 and to know more specific interest of mycorrhizae research in Indonesia within the last 10 years. Data were collected from Garuda Web (https://garuda.kemdikbud.go.id/) a powerful resource platform for discovery of scholarly publications in Indonesia managed by the Ministry of Research, Technology and Higher Education of Indonesia. The results show that within the period of 1980-2000 there are very few articles published and only on Arbuscular mycorrhizal Fungi. The articles grew rapidly during the period of 2010-2020 and consist of Arbuscular mycorrhizal Fungi, Ectomycorrhizae and Orchid mycorrhizae and the most interest aspects studied were on Arbuscular mycorrhizal fungi with emphasis on increasing growth of agriculture plant species. There were 44 agriculture plant species, 29 forestry plant species 16 horticulture plant species and 8 animal feed plant species studied related with Arbuscular mycorrhizal Fungi. Whereas for Ectomycorrhizae there were 7 forestry plant species studied and 6 orchid species studied for orchid mycorrhizae.
Keyword: mychorriza, number of articles, research developments, plant species studied
INTRODUCTION
Mycorrhiza is a form of mutualistic symbiosis between fungi in the soil and the roots of higher plants (Smith and Read, 2007). The term mycorrhiza was first coined by Frank (1877), which means a symbiotic relationship between fungi and roots. Subsequent research found various types of mycorrhizae (Frank, 1888), namely ectomycorrhiza, endomycorrhiza and ectendomycorrhizae. Mutualistic symbiosis is shown by the existence of mutually beneficial reciprocity between plants and fungi. Plants get more nutrients and water from the soil due to the influence of the presence of fungi and fungi get photosynthesis from plants (Auge, 2001). Mycorrhiza as a biological fertilizer can increase the absorption of nutrients, especially phosphate and also several macros and micronutrients such as Cu and Zn. Mycorrhizal colonization on plant roots can expand the area of root absorption by the presence of external hyphae that grow and develop through root hairs (Ermavitalini and Sari, 2014).
The increase in nutrients due to the mutualistic symbiosis of plant roots and mycorrhiza causes a significant increase in plant growth because plant nutrition is increased and is also sufficient (Nurhayati 2012). Mycorrhiza as a biological control agent can also be used as an alternative for improving marginal lands. Plant growth on marginal soil with low pH, high Al and Fe content, can be improved when colonized by mycorrhizae. Mycorrhiza can also increase resistance to drought, especially in areas with low rain (Nasution et al., 2017). The roots of mycorrhizal plants on marginal land will recover quickly after the drought period has passed. Apart from that, the direct role of mycorrhiza is to help roots increase water absorption and increase the number of soil microbes needed by plant roots.
The great benefits of mycorrhiza as biofertilizer, especially on marginal soils, the mycorrhiza research in the world was growing quite rapidly (Zhang et al., 2024). Fields of study researched include in the survival and growth of agricultural plants, forest plants, horticultural plants as well as animal feed plants (Abidin et al., 2017; Budi et al., 2020; Afrianti et al., 2019; Ali et al., 2012) due to better facilitation of the uptake of Phosphorus nutrition in acidic soil (Sheikh-Assadi et al., 2023, Khan et al., 2022), increase absorption of Nitrogen (Wang et al., 2018), producing plant growth hormones (Xing et al., 2022), defending root against soil borne diseases (Bachtiar et al., 2010) and contribute to the improvement of physical, chemical and biological aspects of soil properties (Fall et al., 2022).
The development of mycorrhiza research in Indonesia began in 1897, carried out by Janse who observed mycorrhiza on various types of plants in the Cibodas Botanical Gardens. In the period 1887-1980, not much mycorrhiza research was recorded in literature. As information technology develops, searching for mycorrhiza research literature via the internet is becoming easier. The research aims to describe the development of mychorrizal research during the period of 1980 to 2020 and to know more specific interest of mycorrhizae research in Indonesia with emphasis on plants species involved within last 10 years.
MATERIALS AND METHODS
Data collection
Data collection and retrieval were conducted in the Garuda Web (https://garuda.kemdikbud.go.id/) a powerful resource platform for discovery of scholarly publications in Indonesia managed by Ministry of Research, Technology and Higher Education of Indonesia. The specific key word was carrried out on Indonesian language “Mikoriza”, “Ektomikoriza”, “Endomikoriza”, “Arbuskula Mikoriza Fungi”, “Orchid Mikoriza”. All publication data appearing on the Garuda portal with the above keywords are used to analyze the development of mycorrhizal research for the period 1980 to 2020.
Data Analysis
All published data that appears from the Garuda portal is calculated in total and grouped into the Orchid, Ectomycorrhizal and Arbuscular Mycorrhizal Fungi groups. Next, the number of publications using agricultural, forestry and animal feed crops was analyzed. Plant species that have symbiosis with orchids, ectomycorrhizal and arbuscular mycorrhizal fungi are also analyzed. Microsoft Excell, and graphics were used for organizing and analyzing the data.
RESULTS AND DISCUSSION
Number of articles related to mycorrhizae from 1980-2020
The results of the analysis of the development of the number of articles on AMF, ectomycorrhizal and orchid mycorrhizal for the period 1980-2020 are presented in Figure 1. The data in Figure 1 shows that the development of mycorrhizal research has increased every year. AMF is the most widely studied followed by ectomycorrhiza dan orchid mycorrhiza. In the period of 1980-1990 the number of articles on AMF studies was only one and this increased to six articles in the period of 1990-2000, on the other hand, there is no known published article on Ectomycorrhizal and orchid mycorrhiza studies on the period of 1980-2000. In the period of 2000-2010 the total number of articles was 105 consisting of 95 articles on AMF and 10 article on ectomycorrhiza study. In 2010-2020, mycorrhizal research grew rapidly with a total of 542 articles with the research composition dominated by Arbuscular Mycorrhizal Fungi with 516 articles. We did not find any article related to ectendomycorrhizae during the period of 1980-2020. The aspect studied mostly on the effect of mycorrhizae on the plant growth and production of different plants species (467 articles) and 75 articles emphasis on the biodiversity of mycorrhizae in different ecosystems and others aspect.
The number of studies from year to year shows that the most studied of mycorrhiza is the AMF. According to Smith and Read (2007), AMF is a type of endomycorrhiza fungi could form symbiosis with almost 90% of higher plant types in the world. On the other hand, the research work carried on the ectomycorrhizal fungi was very limited, may be due to the limitation of host plants that can be symbiotic with ectomycorrhizal fungi. Smith and Read (2007) stated that almost all the plants upon which ectomycorrhizas develop are perennials. Most of them are the family of Pinaceae, Dipterocarpaceae, Caesalpinioideae and Betulaceae. The orchids mycorrhizal is very rarely studied and there have only been 10 publications in the period of 2010-2020. This is because not many researchers in Indonesia have studied the field of orchids mycorrhiza.
Development of mycorrhizae research during the period of 2010-2020
As shown in Table 1, there is practically no known published articles in the period of 1980-2010, therefore we analyzed in more detail the research topic for the period of 2010-2020. As shown in Figure 2, the pattern of mycorrhizal research development is similar in the period of 1980-2020. The most research from year to year is dominated by the Arbuscular Mycorrhizal Fungi with the highest number of articles published in 2019 are 79 articles but decrease in 2020 only 25 articles and ectomycorrhizal articles with 2 articles published. The total number of orchid mycorrhizal article published along the period of 2010-2020 are 10 articles with the highest number published in 2015.
The detail analysis related to the plant commodities and plant species studied for each type of mycorrhizae are described bellow
Analysis of plant commodities inoculated by Arbuscular mycorrhizal fungi
Arbuscular mycorrhizas fungi are the most common underground symbiosis mutualism between the roots of wide variety of host plants with the fungi in the order Glomales (Zygomycotina) (Smith and Read, 2007). Figure 3 shows that the Indonesian researcher has an interest to study the effect of AMF to the growth and development of wide variety of plants that can be grouped into the agricultural plants, forestry plants, horticultural plants and animal feed plants. The highest articles published were on agricultural plants (44 articles) followed by forestry plants (29 articles), horticultural plants (16 articles) and animal feed plants (8 articles). All the groups of plants was grown in acidic soil. Most of acid soils (ultisol, oxisol) are spread in tropical countries including in Indonesia. According to Subagyo et al., (2004), Indonesian acidic soils approximately as large as 45,794,000 ha are spread over large island and cover almost 25% of total land surface. Kalimantan island has the largest area of acid soil which covers 21,938,000 ha, followed by Sumatera (9,469,000 ha), Maluku and Papua (8,859,000 ha), Sulawesi (4,303,000 ha), Java (1,172,000 ha), and Nusa Tenggara (53,000 ha). Acidic soil can inhibit plant growth and productivity because the soil has the following characteristics: low nutrient content, high acidity with aluminum and Mn toxicity, low organic matter and biodiversity and very low mineralization and nitrification (Kochian et al., 2004). In addition, AMF has considerable potential in increasing the sustainability of agricultural ecosystems through its role in improving plant nutrient cycles (Friese and Allen 1991) and the process for improving soil aggregates (Tisdall, 1991). Therefore, many researchers used the mycorrhizae as biological fertilizer.
The different number of articles published among agricultural plants, forestry plants, horticultural plants and animal feed plants may be due to the different interest and the number of scientists working on this area. The scientist of agricultural plants mostly works in university as well as in research institutes, and the number of agricultural universities and research institutes in Indonesia was more than those in the forestry university.
Growth and production improvement of agricultural plant species inoculated by Arbuscular mycorrhizal fungi
There were 44 agricultural plant species studied related to AMF (Figure 4). The five top articles published were Zea mays (52 articles), Glycine max (44 articles), Capsicum annum (18 articles), Allium ascalonicum (15 articles) and Oryza sativa (15 articles). Zea mays is a primary commodity that contributes significantly to the Indonesian economy and accelerates the development of the nation's agricultural infrastructure. Increasing maize production can be achieved through extensification, which involves utilizing marginal land. Drought stress represents a condition that hinders maize extensification programs on potential land, including drylands. Glycine max, Capsicum annum, Allium ascalonicum and Oryza sativa were also important agricultural plant species that consumed by majority of Indonesian people and commonly produced on marginal land, therefore many researchers became interested to conduct this research. Zea mays growth and production were increased when inoculated with Arbuscular mycorrhizal fungi alone or combined with organic fertilizer or inorganic fertilizer on marginal land (Abidin et al., 2017; Agustin, 2011; Agustinur et al., 2018; Aidil et al., 2014; Ainun et al., 2019).
The inoculation of AMF alone or with combination with organic or inorganic fertilizer also increase the growth and production of Glycine max (Ardiansyah et al., 2014; Herlina et al., 2016; Damanik et al., 2013), Capsicum annum (Agustin et al., 2010; Hadianur et al., 2017; Baedowi et al., 2019; Rahman et al., 2019), Allium ascalonicum (Ansyar et al., 2017; Begananda et al., 2019; Siagian et al., 2018), Oryza sativa (Aziez et al., 2019; Birnandi, 2012; Winata et al., 2014) and others species presented in Figure 4.
Growth improvement Forestry Plant species inoculated by Arbuscular mycorrhizal fungi
There were 29 forestry plants species studied in relation to AMF. The top five forestry plant species that have attention from Indonesian researcher were Anthocepallus cadamba (9 articles), Aquilaria crassna (6 articles), Tectona grandis (5 articles), Falcataria moluccana (5 articles) and Aleurites moluccana (5 articles) as shown in Table 5. Anthocepallus cadamba and Falcataria moluccana known as species widely planted for degraded forest land rehabilitation.
Inoculation of AMF alone or combination with organic or inorganic fertilizers and bacteria in appropriate dosage increase height and diameter growth of Anthocepallus cadamba in various soil medium in the nursery (Budi et al., 2017a; Budi et al., 2017b; Hasimin et al., 2018), Falcataria moluccana (Budi et al., 2020), Aquilaria crassna, Tectona grandis, Aleurites moluccana and others species presented in Figure 5 also positively responsive to AMF inoculation (Ragil and Irianto, 2015ab; Megawati et al., 2019; Rumondang et al., 2011; Rinti et al., 2015, Ristiyanti et al., 2014).
Growth improvement of horticultural plant species inoculated by Arbuscular mycorrhizal fungi
There were 16 horticultural plants species related to arbuscular mycorrhizal research. The top five horticultural plants species were Elaeis guineensis (21 articles), Theobroma cacao (13 articles), Coffea arabica (12 articles), Hevea braziliensis (12 articles), Piper nigrum (10 articles) and Scharum officinarum (10 articles) as shown in Figure 6. All of these plant species have an important economic value and contribute to the Indonesian state income. Most of these plant species were cultivated in acidic soil, therefore the use of AMF could increase their growth and development. Mycorrhiza in general plays an important role in cultivated plants such as horticultural plants. According to Nurlaila (2015), the use of mycorrhiza in cultivated plants has several advantages, including reducing chemical fertilizer input, and improving soil quality both physically, chemically and biologically.
Inoculation of AMF alone or combined with other microorganisms as well as organic or inorganic fertilizers positively enhance the growth of Elaeis guineensis (Lubis et al., 2019; Madusari, 2016; Aminah et al., 2017), Theobroma cacao (Idhan and Nursyamsi, 2016; Kumalawati et al., 2018; Rahmad et al., 2015), Coffea arabica (Islamiyah et al., 2013; Susanto et al., 2014; Sugiarti et al., 2018), Hevea braziliensis (Hanifah et al., 2014; Hanifah et al., 2015ab), Scharum officinarum (Ismayanti et al., 2013; Leovini et al., 2014; Prihantomo et al., 2015).
Growth improvement of animal feed crops species inoculated by Arbuscular mycorrhizal fungi
AMF can also be used as an alternative to environmentally friendly technology to improve the growth and quality of forage for livestock in various soil and environmental conditions. Figure 7 shows the number of studies of forage plants growth influenced by AMF. The number of animal feed crops species studied were dominated by Purariaria phaseoloides and Penisetum purpureum (3 articles), followed by Indigofera zollingeriana (2 articles). Inoculation of AMF alone or with combination with organic or inorganic fertilizers with appropriate dosage increase the production and nutrient content of P. purpureum (Prabudi et al., 2014; Gutteres, 2018), P. phaseoloides (Ali et al., 2010), P. javanica (Ifradi et al., 2018), Indigofera zollingeriana (Laksono and Karyono, 2017; Herlina et al., 2017) and Hymenachne amplexicaulis (Syafira et al., 2015). The research in agreement with Kanno et al., (2006) which has been reported that AMF inoculation can increase the growth and production of forage for tropical livestock. According to Elviwirda et al. (2016), AMF can be used as biofertilizers to help increase land productivity and quality of tropical livestock forage.
Analysis of forestry plant species inoculated by Ectomycorrhiza
Ectomycorrhiza has a very important role in improving the quality of seedlings and stimulating plant growth in the field, especially on marginal land (Darwo and Sugiarti, 2008). Figure 8 shows the forestry species studied, and the number of articles published in the period of 2010-2020. The forestry species dominated by Dipterocarpaceae family such as Shorea pinanga (4 articles), Shorea javanica (4 articles), Shorea chrysophylla (2 articles). Ectomycorrhizal fungi have an important role in improving the quality of growth, especially in tengkawang (Shorea pinanga) plants which are very dependent on ectomycorrhizae (Omon, 2008). Bintoro et al. (2018) stated that the inoculation of ectomycorrhizal inoculum was able to increase the percentage of colonization and Shorea pinanga growth such as increase in height, leaf area, shoot dry weight and total dry weight. Damar gum also known as damar resin or damar white copal is natural resin that come from the Shorea javanica tree or damar tree which is native to Indonesia. Inoculation of Shorea javanica with different inoculum of ectomycorrhizas increases their height and diameter in the nursery (Handayani et al., 2018; Bintoro et al., 2018). Other species studied are Gnetum gnemon (2 articles), Pinus merkusii (2 articles), and Instia bijuga (1 articles). This species also has an economic value from their fruits, wood and resin.
The number of orchid species studied on orchid mycorrhizae
Orchid is one of the ornamental plants which has high ornamental and economic value. Indonesian orchid estimated up to 5,000 species distributed evenly in various regions and some of them are endemic (Wati et al., 2022). According to Agrios (1978), orchid seeds are very small and do not have endosperm, consequently their natural germination cannot occur unless the seeds are infected with mycorrhizal fungi. There is not much orchid research on orchid mycorrhizae in Indonesia. Figure 9 presents the orchid species studied related to orchid mycorrhizae. Only six orchid species were studied namely Spathoglottis sp., Phalaenopsis sp., Dendrobium sp., Ascocentrum miniatum, Vanda sp., and Dendrobium sp. (Soelistijono et al., 2011; Soelistijono et al., 2017; Mufidah et al., 2017; Septirani et al., 2015).
Orchid seed growth naturally becomes a protocorm with dependence on mycorrhiza for the availability of growth nutrients until the plant grows to maturity. Rhizoctonia is a mycorrhizal fungus that can be associated with ground orchids (Athipunyakom and Manoch 2008). Conservation and cultivation of natural orchids cannot be separated from the role of orchid mycorrhizal fungi. The presence of mycorrhiza on orchid roots can have a positive influence on the growth and distribution of orchids (McCormick et al., 2018). Mycorrhizae have a very important role because they have cellulolytic activity which can convert cellulose in the soil into nutrients that can be absorbed by fungi and then utilized by orchids (Henuhili 2016). The nutritional compounds provided by fungi to orchid plants are sugar, vitamins, amino acids and other compounds that have not yet been identified. Other compounds are those produced by Rhizoctonia sp. namely niacin, a vitamin that can accelerate the germination and growth of orchid seeds.
CONCLUSION
The development of mycorrhizal research is growing rapidly in Indonesia. Research on mycorrhiza in the last 10 years has increased quite significantly compared to the number in the previous years. The aspect that is the dominant topic in mycorrhizal research is the AMF aspect with the largest category of increasing growth and the dominant commodity types, namely agriculture, horticulture and forestry.
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Development of Mycorrhizae as Biofertilizer over Four Decades (1980-2020) in Indonesia
ABSTRACT
Mycorrhiza is a symbiotic mutualism among the plant roots with fungi. Its known as biofertilizer. The research aims to describe the development of mychorrizal research during the period of 1980 to 2020 and to know more specific interest of mycorrhizae research in Indonesia within the last 10 years. Data were collected from Garuda Web (https://garuda.kemdikbud.go.id/) a powerful resource platform for discovery of scholarly publications in Indonesia managed by the Ministry of Research, Technology and Higher Education of Indonesia. The results show that within the period of 1980-2000 there are very few articles published and only on Arbuscular mycorrhizal Fungi. The articles grew rapidly during the period of 2010-2020 and consist of Arbuscular mycorrhizal Fungi, Ectomycorrhizae and Orchid mycorrhizae and the most interest aspects studied were on Arbuscular mycorrhizal fungi with emphasis on increasing growth of agriculture plant species. There were 44 agriculture plant species, 29 forestry plant species 16 horticulture plant species and 8 animal feed plant species studied related with Arbuscular mycorrhizal Fungi. Whereas for Ectomycorrhizae there were 7 forestry plant species studied and 6 orchid species studied for orchid mycorrhizae.
Keyword: mychorriza, number of articles, research developments, plant species studied
INTRODUCTION
Mycorrhiza is a form of mutualistic symbiosis between fungi in the soil and the roots of higher plants (Smith and Read, 2007). The term mycorrhiza was first coined by Frank (1877), which means a symbiotic relationship between fungi and roots. Subsequent research found various types of mycorrhizae (Frank, 1888), namely ectomycorrhiza, endomycorrhiza and ectendomycorrhizae. Mutualistic symbiosis is shown by the existence of mutually beneficial reciprocity between plants and fungi. Plants get more nutrients and water from the soil due to the influence of the presence of fungi and fungi get photosynthesis from plants (Auge, 2001). Mycorrhiza as a biological fertilizer can increase the absorption of nutrients, especially phosphate and also several macros and micronutrients such as Cu and Zn. Mycorrhizal colonization on plant roots can expand the area of root absorption by the presence of external hyphae that grow and develop through root hairs (Ermavitalini and Sari, 2014).
The increase in nutrients due to the mutualistic symbiosis of plant roots and mycorrhiza causes a significant increase in plant growth because plant nutrition is increased and is also sufficient (Nurhayati 2012). Mycorrhiza as a biological control agent can also be used as an alternative for improving marginal lands. Plant growth on marginal soil with low pH, high Al and Fe content, can be improved when colonized by mycorrhizae. Mycorrhiza can also increase resistance to drought, especially in areas with low rain (Nasution et al., 2017). The roots of mycorrhizal plants on marginal land will recover quickly after the drought period has passed. Apart from that, the direct role of mycorrhiza is to help roots increase water absorption and increase the number of soil microbes needed by plant roots.
The great benefits of mycorrhiza as biofertilizer, especially on marginal soils, the mycorrhiza research in the world was growing quite rapidly (Zhang et al., 2024). Fields of study researched include in the survival and growth of agricultural plants, forest plants, horticultural plants as well as animal feed plants (Abidin et al., 2017; Budi et al., 2020; Afrianti et al., 2019; Ali et al., 2012) due to better facilitation of the uptake of Phosphorus nutrition in acidic soil (Sheikh-Assadi et al., 2023, Khan et al., 2022), increase absorption of Nitrogen (Wang et al., 2018), producing plant growth hormones (Xing et al., 2022), defending root against soil borne diseases (Bachtiar et al., 2010) and contribute to the improvement of physical, chemical and biological aspects of soil properties (Fall et al., 2022).
The development of mycorrhiza research in Indonesia began in 1897, carried out by Janse who observed mycorrhiza on various types of plants in the Cibodas Botanical Gardens. In the period 1887-1980, not much mycorrhiza research was recorded in literature. As information technology develops, searching for mycorrhiza research literature via the internet is becoming easier. The research aims to describe the development of mychorrizal research during the period of 1980 to 2020 and to know more specific interest of mycorrhizae research in Indonesia with emphasis on plants species involved within last 10 years.
MATERIALS AND METHODS
Data collection
Data collection and retrieval were conducted in the Garuda Web (https://garuda.kemdikbud.go.id/) a powerful resource platform for discovery of scholarly publications in Indonesia managed by Ministry of Research, Technology and Higher Education of Indonesia. The specific key word was carrried out on Indonesian language “Mikoriza”, “Ektomikoriza”, “Endomikoriza”, “Arbuskula Mikoriza Fungi”, “Orchid Mikoriza”. All publication data appearing on the Garuda portal with the above keywords are used to analyze the development of mycorrhizal research for the period 1980 to 2020.
Data Analysis
All published data that appears from the Garuda portal is calculated in total and grouped into the Orchid, Ectomycorrhizal and Arbuscular Mycorrhizal Fungi groups. Next, the number of publications using agricultural, forestry and animal feed crops was analyzed. Plant species that have symbiosis with orchids, ectomycorrhizal and arbuscular mycorrhizal fungi are also analyzed. Microsoft Excell, and graphics were used for organizing and analyzing the data.
RESULTS AND DISCUSSION
Number of articles related to mycorrhizae from 1980-2020
The results of the analysis of the development of the number of articles on AMF, ectomycorrhizal and orchid mycorrhizal for the period 1980-2020 are presented in Figure 1. The data in Figure 1 shows that the development of mycorrhizal research has increased every year. AMF is the most widely studied followed by ectomycorrhiza dan orchid mycorrhiza. In the period of 1980-1990 the number of articles on AMF studies was only one and this increased to six articles in the period of 1990-2000, on the other hand, there is no known published article on Ectomycorrhizal and orchid mycorrhiza studies on the period of 1980-2000. In the period of 2000-2010 the total number of articles was 105 consisting of 95 articles on AMF and 10 article on ectomycorrhiza study. In 2010-2020, mycorrhizal research grew rapidly with a total of 542 articles with the research composition dominated by Arbuscular Mycorrhizal Fungi with 516 articles. We did not find any article related to ectendomycorrhizae during the period of 1980-2020. The aspect studied mostly on the effect of mycorrhizae on the plant growth and production of different plants species (467 articles) and 75 articles emphasis on the biodiversity of mycorrhizae in different ecosystems and others aspect.
The number of studies from year to year shows that the most studied of mycorrhiza is the AMF. According to Smith and Read (2007), AMF is a type of endomycorrhiza fungi could form symbiosis with almost 90% of higher plant types in the world. On the other hand, the research work carried on the ectomycorrhizal fungi was very limited, may be due to the limitation of host plants that can be symbiotic with ectomycorrhizal fungi. Smith and Read (2007) stated that almost all the plants upon which ectomycorrhizas develop are perennials. Most of them are the family of Pinaceae, Dipterocarpaceae, Caesalpinioideae and Betulaceae. The orchids mycorrhizal is very rarely studied and there have only been 10 publications in the period of 2010-2020. This is because not many researchers in Indonesia have studied the field of orchids mycorrhiza.
Development of mycorrhizae research during the period of 2010-2020
As shown in Table 1, there is practically no known published articles in the period of 1980-2010, therefore we analyzed in more detail the research topic for the period of 2010-2020. As shown in Figure 2, the pattern of mycorrhizal research development is similar in the period of 1980-2020. The most research from year to year is dominated by the Arbuscular Mycorrhizal Fungi with the highest number of articles published in 2019 are 79 articles but decrease in 2020 only 25 articles and ectomycorrhizal articles with 2 articles published. The total number of orchid mycorrhizal article published along the period of 2010-2020 are 10 articles with the highest number published in 2015.
The detail analysis related to the plant commodities and plant species studied for each type of mycorrhizae are described bellow
Analysis of plant commodities inoculated by Arbuscular mycorrhizal fungi
Arbuscular mycorrhizas fungi are the most common underground symbiosis mutualism between the roots of wide variety of host plants with the fungi in the order Glomales (Zygomycotina) (Smith and Read, 2007). Figure 3 shows that the Indonesian researcher has an interest to study the effect of AMF to the growth and development of wide variety of plants that can be grouped into the agricultural plants, forestry plants, horticultural plants and animal feed plants. The highest articles published were on agricultural plants (44 articles) followed by forestry plants (29 articles), horticultural plants (16 articles) and animal feed plants (8 articles). All the groups of plants was grown in acidic soil. Most of acid soils (ultisol, oxisol) are spread in tropical countries including in Indonesia. According to Subagyo et al., (2004), Indonesian acidic soils approximately as large as 45,794,000 ha are spread over large island and cover almost 25% of total land surface. Kalimantan island has the largest area of acid soil which covers 21,938,000 ha, followed by Sumatera (9,469,000 ha), Maluku and Papua (8,859,000 ha), Sulawesi (4,303,000 ha), Java (1,172,000 ha), and Nusa Tenggara (53,000 ha). Acidic soil can inhibit plant growth and productivity because the soil has the following characteristics: low nutrient content, high acidity with aluminum and Mn toxicity, low organic matter and biodiversity and very low mineralization and nitrification (Kochian et al., 2004). In addition, AMF has considerable potential in increasing the sustainability of agricultural ecosystems through its role in improving plant nutrient cycles (Friese and Allen 1991) and the process for improving soil aggregates (Tisdall, 1991). Therefore, many researchers used the mycorrhizae as biological fertilizer.
The different number of articles published among agricultural plants, forestry plants, horticultural plants and animal feed plants may be due to the different interest and the number of scientists working on this area. The scientist of agricultural plants mostly works in university as well as in research institutes, and the number of agricultural universities and research institutes in Indonesia was more than those in the forestry university.
Growth and production improvement of agricultural plant species inoculated by Arbuscular mycorrhizal fungi
There were 44 agricultural plant species studied related to AMF (Figure 4). The five top articles published were Zea mays (52 articles), Glycine max (44 articles), Capsicum annum (18 articles), Allium ascalonicum (15 articles) and Oryza sativa (15 articles). Zea mays is a primary commodity that contributes significantly to the Indonesian economy and accelerates the development of the nation's agricultural infrastructure. Increasing maize production can be achieved through extensification, which involves utilizing marginal land. Drought stress represents a condition that hinders maize extensification programs on potential land, including drylands. Glycine max, Capsicum annum, Allium ascalonicum and Oryza sativa were also important agricultural plant species that consumed by majority of Indonesian people and commonly produced on marginal land, therefore many researchers became interested to conduct this research. Zea mays growth and production were increased when inoculated with Arbuscular mycorrhizal fungi alone or combined with organic fertilizer or inorganic fertilizer on marginal land (Abidin et al., 2017; Agustin, 2011; Agustinur et al., 2018; Aidil et al., 2014; Ainun et al., 2019).
The inoculation of AMF alone or with combination with organic or inorganic fertilizer also increase the growth and production of Glycine max (Ardiansyah et al., 2014; Herlina et al., 2016; Damanik et al., 2013), Capsicum annum (Agustin et al., 2010; Hadianur et al., 2017; Baedowi et al., 2019; Rahman et al., 2019), Allium ascalonicum (Ansyar et al., 2017; Begananda et al., 2019; Siagian et al., 2018), Oryza sativa (Aziez et al., 2019; Birnandi, 2012; Winata et al., 2014) and others species presented in Figure 4.
Growth improvement Forestry Plant species inoculated by Arbuscular mycorrhizal fungi
There were 29 forestry plants species studied in relation to AMF. The top five forestry plant species that have attention from Indonesian researcher were Anthocepallus cadamba (9 articles), Aquilaria crassna (6 articles), Tectona grandis (5 articles), Falcataria moluccana (5 articles) and Aleurites moluccana (5 articles) as shown in Table 5. Anthocepallus cadamba and Falcataria moluccana known as species widely planted for degraded forest land rehabilitation.
Inoculation of AMF alone or combination with organic or inorganic fertilizers and bacteria in appropriate dosage increase height and diameter growth of Anthocepallus cadamba in various soil medium in the nursery (Budi et al., 2017a; Budi et al., 2017b; Hasimin et al., 2018), Falcataria moluccana (Budi et al., 2020), Aquilaria crassna, Tectona grandis, Aleurites moluccana and others species presented in Figure 5 also positively responsive to AMF inoculation (Ragil and Irianto, 2015ab; Megawati et al., 2019; Rumondang et al., 2011; Rinti et al., 2015, Ristiyanti et al., 2014).
Growth improvement of horticultural plant species inoculated by Arbuscular mycorrhizal fungi
There were 16 horticultural plants species related to arbuscular mycorrhizal research. The top five horticultural plants species were Elaeis guineensis (21 articles), Theobroma cacao (13 articles), Coffea arabica (12 articles), Hevea braziliensis (12 articles), Piper nigrum (10 articles) and Scharum officinarum (10 articles) as shown in Figure 6. All of these plant species have an important economic value and contribute to the Indonesian state income. Most of these plant species were cultivated in acidic soil, therefore the use of AMF could increase their growth and development. Mycorrhiza in general plays an important role in cultivated plants such as horticultural plants. According to Nurlaila (2015), the use of mycorrhiza in cultivated plants has several advantages, including reducing chemical fertilizer input, and improving soil quality both physically, chemically and biologically.
Inoculation of AMF alone or combined with other microorganisms as well as organic or inorganic fertilizers positively enhance the growth of Elaeis guineensis (Lubis et al., 2019; Madusari, 2016; Aminah et al., 2017), Theobroma cacao (Idhan and Nursyamsi, 2016; Kumalawati et al., 2018; Rahmad et al., 2015), Coffea arabica (Islamiyah et al., 2013; Susanto et al., 2014; Sugiarti et al., 2018), Hevea braziliensis (Hanifah et al., 2014; Hanifah et al., 2015ab), Scharum officinarum (Ismayanti et al., 2013; Leovini et al., 2014; Prihantomo et al., 2015).
Growth improvement of animal feed crops species inoculated by Arbuscular mycorrhizal fungi
AMF can also be used as an alternative to environmentally friendly technology to improve the growth and quality of forage for livestock in various soil and environmental conditions. Figure 7 shows the number of studies of forage plants growth influenced by AMF. The number of animal feed crops species studied were dominated by Purariaria phaseoloides and Penisetum purpureum (3 articles), followed by Indigofera zollingeriana (2 articles). Inoculation of AMF alone or with combination with organic or inorganic fertilizers with appropriate dosage increase the production and nutrient content of P. purpureum (Prabudi et al., 2014; Gutteres, 2018), P. phaseoloides (Ali et al., 2010), P. javanica (Ifradi et al., 2018), Indigofera zollingeriana (Laksono and Karyono, 2017; Herlina et al., 2017) and Hymenachne amplexicaulis (Syafira et al., 2015). The research in agreement with Kanno et al., (2006) which has been reported that AMF inoculation can increase the growth and production of forage for tropical livestock. According to Elviwirda et al. (2016), AMF can be used as biofertilizers to help increase land productivity and quality of tropical livestock forage.
Analysis of forestry plant species inoculated by Ectomycorrhiza
Ectomycorrhiza has a very important role in improving the quality of seedlings and stimulating plant growth in the field, especially on marginal land (Darwo and Sugiarti, 2008). Figure 8 shows the forestry species studied, and the number of articles published in the period of 2010-2020. The forestry species dominated by Dipterocarpaceae family such as Shorea pinanga (4 articles), Shorea javanica (4 articles), Shorea chrysophylla (2 articles). Ectomycorrhizal fungi have an important role in improving the quality of growth, especially in tengkawang (Shorea pinanga) plants which are very dependent on ectomycorrhizae (Omon, 2008). Bintoro et al. (2018) stated that the inoculation of ectomycorrhizal inoculum was able to increase the percentage of colonization and Shorea pinanga growth such as increase in height, leaf area, shoot dry weight and total dry weight. Damar gum also known as damar resin or damar white copal is natural resin that come from the Shorea javanica tree or damar tree which is native to Indonesia. Inoculation of Shorea javanica with different inoculum of ectomycorrhizas increases their height and diameter in the nursery (Handayani et al., 2018; Bintoro et al., 2018). Other species studied are Gnetum gnemon (2 articles), Pinus merkusii (2 articles), and Instia bijuga (1 articles). This species also has an economic value from their fruits, wood and resin.
The number of orchid species studied on orchid mycorrhizae
Orchid is one of the ornamental plants which has high ornamental and economic value. Indonesian orchid estimated up to 5,000 species distributed evenly in various regions and some of them are endemic (Wati et al., 2022). According to Agrios (1978), orchid seeds are very small and do not have endosperm, consequently their natural germination cannot occur unless the seeds are infected with mycorrhizal fungi. There is not much orchid research on orchid mycorrhizae in Indonesia. Figure 9 presents the orchid species studied related to orchid mycorrhizae. Only six orchid species were studied namely Spathoglottis sp., Phalaenopsis sp., Dendrobium sp., Ascocentrum miniatum, Vanda sp., and Dendrobium sp. (Soelistijono et al., 2011; Soelistijono et al., 2017; Mufidah et al., 2017; Septirani et al., 2015).
Orchid seed growth naturally becomes a protocorm with dependence on mycorrhiza for the availability of growth nutrients until the plant grows to maturity. Rhizoctonia is a mycorrhizal fungus that can be associated with ground orchids (Athipunyakom and Manoch 2008). Conservation and cultivation of natural orchids cannot be separated from the role of orchid mycorrhizal fungi. The presence of mycorrhiza on orchid roots can have a positive influence on the growth and distribution of orchids (McCormick et al., 2018). Mycorrhizae have a very important role because they have cellulolytic activity which can convert cellulose in the soil into nutrients that can be absorbed by fungi and then utilized by orchids (Henuhili 2016). The nutritional compounds provided by fungi to orchid plants are sugar, vitamins, amino acids and other compounds that have not yet been identified. Other compounds are those produced by Rhizoctonia sp. namely niacin, a vitamin that can accelerate the germination and growth of orchid seeds.
CONCLUSION
The development of mycorrhizal research is growing rapidly in Indonesia. Research on mycorrhiza in the last 10 years has increased quite significantly compared to the number in the previous years. The aspect that is the dominant topic in mycorrhizal research is the AMF aspect with the largest category of increasing growth and the dominant commodity types, namely agriculture, horticulture and forestry.
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