Home Effect of arbuscular mycorrhizal fungi on early growth, root colonization, and chlorophyll content of North Maluku nutmeg cultivars
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Effect of arbuscular mycorrhizal fungi on early growth, root colonization, and chlorophyll content of North Maluku nutmeg cultivars

  • Wawan Sulistiono EMAIL logo , Himawan Bayu Aji , Sigid Handoko , Jonathan Anugrah Lase , Suryanti Suryanti , Yayan Apriyana and Molide Rizal
Published/Copyright: August 29, 2023
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Open Agriculture
From the journal Open Agriculture Volume 8 Issue 1

Abstract

This study aimed to investigate the agronomic traits of nutmeg transplanting by arbuscular mycorrhizal fungi (AMF) inoculation. The low-fertility soil of Sofifi North Maluku was subjected to a slow early growth stage of nutmeg cultivars. A completely randomized design was used in the experiment. The first factor was three different AMF doses: 0, 4, and 8 g seedlings−1. The second factor consisted of three cultivars: “Ternate 1,” “Tobelo 1,” and “Makian.” Root colonization and agronomic traits were measured 28 weeks after inoculation and transplantation. Results showed that AMF inoculation increased the AM colonization by 2.5–39.0%, significantly increased the leaf area (LA) (p < 0.01) in all cultivars, and interacted with cultivars to increase chlorophyll a (Chl a) (p < 0.05), chlorophyll b (Chl b) (p < 0.01), and total Chl (p < 0.01). Cultivars “Makian” showed the highest Chl (188.4%) at 8 g seedling−1 doses of AMF that were significantly (p < 0.01) different from the cultivar “Tobelo 1” at the same dose. The largest mycorrhizal response was found in the cultivar “Ternate 1” (biomass increase of 30–37.0%). The cultivar “Ternate 1” produced the largest LA (36.7–106.9%) and shoot dry weight (27.8–45.8%) that were significantly (p < 0.01) different from the other cultivars. The percentage of AM colonization was strongly determined (R 2 = 0.88) by Chl a, Chl b, and K content in leaves. This technology is a breakthrough to increase LA and plant biomass in the early growth stage of nutmeg cultivation.

Keywords: AMF inoculation; biomass; chlorophyll; growth; nutmeg cultivars; root colonization

1 Introduction

Nutmeg (Myristica fragrans Houtt.), endemic to Indonesia, has a long history of use as a spice and freshener, which has since spread mainly to India and Madagascar [1]. Numerous benefits of nutmeg include its use in medicine, as an essential oil, and in food flavoring [2]. Significant advantages and localized growth have made Indonesia a world leader in nutmeg production [1,3]. In North Maluku, nutmeg is a major commodity that generates the region’s primary income [4]. The economic parts of nutmeg are generally the seeds and the mace.

Several cultivars of nutmeg originate from the northern islands of Maluku, notably, “Ternate 1,” “Tidore 1,” “Tobelo 1,” “Makian,” and “Patani” [5]. Nutmeg is grown in home gardens, cultivated using an agroforestry system, or mixed with over 30 years old coconuts (mixed gardens) [5,6]. However, approximately 5% of the old and damaged nutmeg plantations occur in North Maluku [3,4]. Therefore, plant rejuvenation is required to maintain and increase plantation productivity.

Unfortunately, information on transplantation techniques to support plant growth in rejuvenation/regeneration has not been widely disseminated. This is important because nutmegs show slow early growth in the field, exposing them to drought stress or high temperatures and weeds [5,7].

To cope with the stress of drought and soil fertility, transplant techniques and suitable cultivars are required to accelerate growth [8,9]. Cultivation is necessary to allow the use of applications that can enhance plant growth while maintaining soil fertility for sustainable agriculture. For instance, the exogenous application of nanofertilizers to horticultural crops improved the tolerance and mitigation of salt stress [10]. However, biological approaches would be more environmentally friendly to adopt rather than chemical ones. One such approach is using arbuscular mycorrhizal fungi (AMF), which has been shown to improve plant performance and soil health [11,12,13]. AMF plays a vital role in enhancing phosphorus uptake in plants [14] and increasing salt stress tolerance [15].

AMF colonization is of utmost importance for plant growth and soil conditions [12,16]. The effect of AMF on plants was shown in cocoa and coffee seedlings. Cocoa and coffee seedlings experienced an increase in height by 50.58 and 27.29%, respectively, and an increase in shoot dry weight (SDW) by 127.55 and 121.21%, respectively, compared to the absence of AMF inoculation [16]. In terms of plant growth, AMF increases rooting capacity, post-transplant growth, biomass weight, and seed biomass [17–19]. The colonization of AMF protects plants against environmental stresses, such as reducing the stress effect of nickel metal (Ni) which can result in enhanced metabolism, physiological disorders, and plant mortality [20].

Research on the growth of transplanted nutmeg seedlings by Abirami et al. [21] indicates that the treatment of growth media increases the seedling height, girth, number of leaves, shoot length, root length (RL), and plant biomass. Moreover, Abirami et al. [21] identified a superior growth medium for the early growth of nutmeg seedlings, comprising a mixture of soil, coir dust, sand, and vermicompost in a 1:1:1:1 composition ratio. Furthermore, the inoculation of a biofertilizer containing 0.3% phosphate-solubilizing bacteria (Bacillus) resulted in even higher plant growth, wider leaf area (LA), and improved soil microbial activity for nutmeg seedlings at 24 weeks after transplanting [7].

However, a sustainable biological input is needed. Seedling growth capacity is positively affected by the colonization of AMF [16]. Loit et al. [12] reported that AMF colonization was more pronounced in organic rather than conventional farms. The incorporation of microbes (bacteria and fungi) has been widely reported to enhance soil fertility, plant growth and development, and crops yields, along with improved plant quality and soil texture [21,22,23]; for example, AMF in the planting medium, in addition to the treatment that has been carried out [24] and biological fertilizers containing beneficial bacteria [7].

The AMF-inoculated Gleditsia sinensis Lam has the potential to promote root properties [19]. Moreover, it is reported that in sugarcane, inoculation with AMF provides other advantages in terms of Chl, net assimilation rate, and plant growth rate [17].

To date, the effects of these mycorrhizae vary among varieties [25]. In addition, the level of colonization, the density of the spores, and the density of the dynamic length of the hyphae depend on the season, biodiversity–ecosystem function [26,27], and AMF species [28]. According to Arias et al. [29] and Martins and Rodrigues [30], the development of AMF is influenced by ecosystems, ecology, and cultivation practices. Meanwhile, the adaptability of the plant to the soil will determine its ability for colonization [31]. However, the effect of mycorrhiza on the early growth of nutmeg varieties is rarely reported.

This experiment helps to identify cultivars' agronomic and physiological features with enhanced mycorrhizal response (MR). The objective of this research is to develop a method to enhance the early development of nutmeg. The results will be helpful for the establishment of a broader and more suitable central nutmeg zone.

2 Materials and methods

2.1 Plant culture and AMF inoculation treatment

The research was conducted in the plantation seedlings area of the Assessment Institute of Agricultural Technology (AIAT) of North Maluku, Indonesia (5 m above sea level [a.s.l.]) from August 2019 to May 2021. The treatment site was located at 0°41′38.17″N; 127°33′15.18″E. The region’s agro climate according to Schmidt–Ferguson’s classification belongs to humid (0.143 < Q < 0.333) [26]. In 2021, the monthly precipitation in January, February, March, April, May, June, July, August, September, October, November, and December was 306.6, 927.9, 839.4, 1154.5, 931.4, 621.8, 1119.2, 993.4, 632.5, 832.3, 861.2, and 945.4 mm, respectively. In 2021, the monthly average temperature was 27.1°C (maximum: 30.9°C, minimum: 24.0°C). The monthly sunshine duration (%) in 2021 was 43.53% [32,33].

The experiment was conducted using a factorial completely randomized design (CRD) arranged in a 3 × 3 factorial with seven replications per treatment combination. The first factor was nutmeg cultivars consisting of “Makian” (V1), “Tobelo 1” (V2), and “Ternate 1” (V3). The second factor was AMF inoculum application doses, which were 0 (control), 4, and 8 g seedlings−1. There were nine treatment combinations and seven seedlings per treatment combination. The treatment dosage range was determined based on the findings from a previous study by Sulistiono et al. [18], which demonstrated that the application of 2–4 g of AMF inoculum per seedling would significantly increase root/shoot growth. The increase was evident in parameters such as RL, root surface area (RSA), and the number of sugarcane shoot roots. Additionally, as reported by Sulistiono et al. [34], the application of 2–4 g AMF inoculum per coconut seedlings (combined with an NPK fertilizer, 6 g of seeds−1) resulted in a significant enhancement of RSA (p < 0.05) compared to a non-mycorrhizal control.

This work was conducted on an open ground of the AIAT experimental site in North Maluku. The age of the transplanted seedlings was 11 months after germination. Nutmeg seedlings of three cultivars were obtained from selected mother tree seeds, which were first germinated at the shade house germination seedlings location. When the seeds germinated, the seeds were transplanted to seedling polybags measuring 17 mm × 20 mm × 0.06 mm. Seedlings were placed in a nursery location in a shade house with an absorption capacity of 40%. Nutmeg seedlings are retained for 9 months until they are ready to be transplanted into the field.

The experiment was carried out by transplanting the nutmeg seedlings to transplanting polybags (large-sized polybags, 50 × 50 cm). In total, there were 63 polybags. The soil medium for seedling transplantation was taken from non-sterilized soil in the nursery. The type of soil in the research location was Alluvial based on the Bogor Soil Research Center (1983) classification system [35]. The soil’s chemical properties were measured as follows: pH 5.46, C-organic 1.79%, N total 0.77%, available P (P2O5) 266 ppm, and available K 208 ppm. The pH (H2O) was determined using a pH meter with a 1:5 soil/water ratio (method lK. 5.4.c). Organic carbon (C-organic) content was measured using the Walkley and Black method (method 1 K.5.4.d). Total nitrogen (N-total) was determined using the Kjeldahl method (method1K.5.4.e). Available potassium (K) was analyzed using the Morgan–Wolf method, and available phosphorus (P2O5) was determined using the Olsen method 1K.5.4.h (analyzed in Plant Laboratory of AIAT Yogyakarta). Soil analysis was performed after 2 weeks of AMF inoculation.

The AMF inoculum was in the form of zeolite granular media (a commercial arbuscular mycorrhizal [AM] inoculum). AMF inoculation was carried out 1 week after transplanting. According to the treatment combination, mycorrhizal counts of 3.6 spores g−1 granular zeolite media by spreading AMF inoculum to soil media in polybags. The segregated AMF genera were Glomus sp., Funneliformis sp., Acaulospora sp., Gigaspora sp., and Scutellospora sp.

AMF originated from the rhizosphere of plantations in Java. AMF was propagated by trapping soil and compost with a ratio of 9.5:0.5 followed by sterilization (autoclaved at 121°C for 45 min at 1 atm pressure). The sterilized soil media were then planted and retained for 2.5 months. Then, the planting medium was harvested and dried. The roots were cut into pieces and then mixed with a carrier medium, namely zeolite granules. The AMF cultures used were mycorrhizal spores in zeolite media and root pieces.

3 Seedling transplantation and plant cultivation

Nutmeg seedlings planted in polybags measuring 17 cm × 20 cm and 9 months old in the nursery were transplanted to polybags measuring 50 cm × 50 cm in a soil volume of 25 kg. The polybags for seedlings transplanting were arranged at a distance of 1 m × 1 m for each treatment combination according to the factorial CRD (Figure 1).

Figure 1 The layout of the treatment polybags and the growth performance of nutmeg after transplanting the seedlings. Polybags for transplanting seedlings were arranged in a 3 × 3 factorial of CRD with seven sample plants per treatment combination for a total of 63 polybags.
Figure 1

The layout of the treatment polybags and the growth performance of nutmeg after transplanting the seedlings. Polybags for transplanting seedlings were arranged in a 3 × 3 factorial of CRD with seven sample plants per treatment combination for a total of 63 polybags.

Seedlings were transplanted by tearing the seed polybags to dispose of the plastic. Nutmeg seedlings with soil-covered roots are transplanted in polybags and water immediately. Plants were treated until the age of 28 weeks after inoculation and transplantation (WAI-P). Plant treatments in this work were as follows: (1) weed control was carried out by mechanically removing weeds from the soil in polybags and cleaning the grass in the soil locations between polybags; (2) watering using a hose was carried out every 5 days; (3) chemical or organic fertilization was not applied to the nutmeg seeds plantation; and (4) spraying for pest or disease control was not deployed.

3.1 Measurements

Measurements were made on several parameters of growth, physiology, and colonization at 28 WAI-P. The observed parameters included the root colonization, LA, chlorophyll a (Chl a), chlorophyll b (Chl b), Chl (Chl a + Chl b), as well as biomass weight, RSA, RL, SDW, root dry weight (RDW), proline content in leaf (PRO-l), nitrate reductase activity (NRA) in leaf, nitrogen (N), phosphorus (P), and potassium (K) contents in leaves, and MR.

Root colonization by AMF was evaluated using clearing and staining methods, following the procedures of Kormanik and McGraw [36]. Root samples were washed carefully using running water and then cut into 1 cm-long pieces (100 cuttings per treatment unit). The roots were cleared in hot 10% KOH and neutralized with 1% HCl. Root staining was done by dipping the root pieces using trypan blue (0.05% w/v dissolved in a solution of 5% lactic acid, 50% glycerol, and 45% water) for 24 h. Roots infected with AMF were observed for 100 root pieces using a light microscope Olympic CX31 connected to an Optilab camera at a magnification of 400×. The percentage of mycorrhizal colonization was calculated based on the following formula [37]:

(1) Percentage root infected = ( Number root infected/Number root observed ) × 100 .

Seven plants per treatment unit were observed at 28 WAI-P. The Chl a, Chl b, and Chl were measured using Winterman and de Monts’ method [38] at 28 WAI-P. Measurements of NRA, PRO-l, RSA, RL, SDW, and RDW were performed at 28 WAI-P at the Faculty of Agriculture Plant Production Laboratory, Universitas Gadjah Mada (UGM), Yogyakarta, Indonesia. Leaf NRA content was measured using Hartiko’s method, as modified by Indradewa et al. [39]. PRO-l was determined using the “ninhydrin” procedure described by Bates et al. [40].

The RL and RSA were measured using an area meter. The data analysis was performed using the line intersection method developed by Tennant [41], which was further refined by Indradewa [42] as described in Sulistiono et al. [18]. To calculate the roots’ surface area, the roots were assumed to be cylindrical, and the root projection area was defined as two times the product of the RL (L), and the radius (R) = 2 RL. The RSA was then determined as the exposed surface of the cylinder bark without cover at both root edges, calculated as the circumference multiplied by the RL = 2πRL

SDW and RDW measurements were obtained by drying the collected plant samples in an oven set at 75°C. Each sample plant was cut to a length of 15 cm and placed in a paper envelope. The paper envelope containing the plant biomass was then subjected to oven drying until a constant weight was reached, typically taking approximately 5 days. To calculate SDW, the weights of the shoot parts, including the stem above the ground, twigs, and leaves, were individually measured and then summed together. On the other hand, RDW was calculated by weighing and summing the weight of all root parts, which include the root base and branches.

The LA was measured at the age of 28 WAI-P. The measurement was conducted using an LA meter in the Plant Production Laboratory of the Faculty of Agriculture, UGM, Yogyakarta, Indonesia.

The N, P, and K contents were observed in leaves at 28 WAI-P in the plant laboratory of AIAT Yogyakarta. The N concentration in the leaves was measured using the Kjeldahl method. The dry ashing method was employed for P and K concentration analysis, utilizing HNO3 and HClO4 solutions. The P concentration was measured using a UV–Vis spectrophotometer, while the K concentration was determined using an Atomic Absorption spectrophotometer. The chemical analysis followed the procedures outlined by Yoshida et al. [43] (analyzed in the Plant Laboratory of AIAT Yogyakarta).

In this study, the MR was measured as the total dry weight of plant biomass. The MR for the total dry weight of biomass was calculated for every cultivar inoculated by AMF using the following formula:

(2) MR ( % ) = ln ( i / i i ) ,

where i is the total dry weight of biomass of mycorrhizal plants and ii is the total dry weight of biomass of non-mycorrhizal plants [31].

3.2 Data analysis

Data were analyzed using the factorial CRD ANOVA using the SAS 9 program for Windows (SAS Institute, Cary, NC, USA). If there was an interaction between factors, the interaction effects were compared. If not, the treatment endpoints were compared according to the representative results of Duncan’s multiple-interval test at p < 0.05. Stepwise regression was also performed on agronomic traits to identify the determinants of colonization ability.

4 Results

4.1 Colonization

An interaction between AMF inoculation doses and cultivars was observed, significantly affecting colonization (p < 0.01) (Table 1). The cultivar “Makian” at AMF doses of 8 g seedling−1 resulted in much higher AM colonization (350–576%) than other cultivars following the same dose (Table 2).

Table 1

ANOVA test of colonization, physiology, and plant growth parameters at 28 WAI_P

Source df Pr > F
Colonization Chl a Chl b Chl LA SDW RL [K] in leaves
Cultivars (C) 2 <0.0001 0.0029 0.0340 0.0051 0.0002 <0.0001 0.0198 0.0007
Mycorrhizae (M) 2 <0.0001 0.5493 0.3603 0.4306 0.1383 0.2140 0.7945 0.0092
C*M 4 0.0004 0.0264 0.0070 0.0100 0.1017 0.1651 0.7581 0.1727
CV (%) 21.96 3.91 4.22 5.78 21.96 20.97 19.42 6.08
Table 2

Effect of combined cultivars and dose of AMF on mycorrhizal colonization on nutmeg plant roots at 28 WAI-P

Cultivars Doses of AMF Colonization*
g seedling−1 %
Myristica fragrans “Makian” 0 17.00b
Myristica fragrans “Makian” 4 5.00cd
Myristica fragrans “Makian” 8 18.00b
Myristica fragrans “Tobelo 1” 0 39.00a
Myristica fragrans “Tobelo 1” 4 15.00b
Myristica fragrans “Tobelo 1” 8 4.00cd
Myristica fragrans “Ternate 1” 0 10.00bc
Myristica fragrans “Ternate 1” 4 2.00d
Myristica fragrans “Ternate 1” 8 2.66d

*Numbers followed by the same letters in the same column did not differ significantly at p < 0.05 according to Duncanʼs multiple range test.

This condition indicated that the cultivar “Makian” was the most suitable for AMF inoculation. These results indicate that the compatibility between the AMF inoculation doses and the specific cultivar influences the colonization ability of AMF during the early growth of nutmeg.

The cultivar “Makian” appeared to be more responsive to mycorrhizal inoculations than other cultivars. Figure 2 illustrates the colonization of roots infected with AMF.

Figure 2 (a and b) Nutmeg root infected by AMF. IH, internally hyphae. Scale bar: 10 µm. Objective 10×.
Figure 2

(a and b) Nutmeg root infected by AMF. IH, internally hyphae. Scale bar: 10 µm. Objective 10×.

4.2 Plant physiology

Chlorophyll. The interaction between cultivar and AMF inoculation dose was significant (p < 0.05) for Chl a, Chl b, and Chl (Table 1). The cultivar “Makian” at an AMF dose of 8 g seedling−1 produced the highest Chl a, Chl b, and Chl, which differed considerably from other treatment combinations, except cultivar “Ternate 1” at a dose of 4–8 g seedling−1 AMF and the cultivar “Makian” at a dose of 0 g seedling−1. However, the combined treatment of cultivar “Makian” at 8 g seedling−1 dose produced the highest Chl a (17.0–158.6%), Chl b (34.9–231.5%), and Chl (32.4–188.4%) compared to other treatment combinations (Table 3). These indicated that the AMF dose of 8 g seedling−1 can be applied to increase the foliar chlorophyll content of cultivar “Makian.” In contrast, other cultivars required an increase in the dose of AMF.

Table 3

Effect of combined treatment of cultivars and doses of AMF on leaf chlorophyll content at 28 WAI-P

Cultivars Doses of AMF Chl a Chl b Chl
g seedling−1 mg g−1 mg g−1 mg g−1
Myristica fragrans “Makian” 0 0.294ab 0.167ab 0.461ab
Myristica fragrans “Makian” 4 0.224b–d 0.131bc 0.356bc
Myristica fragrans “Makian” 8 0.344a 0.305a 0.649a
Myristica fragrans “Tobelo 1” 0 0.208b–d 0.152bc 0.360bc
Myristica fragrans “Tobelo 1” 4 0.190b–d 0.127bc 0.318bc
Myristica fragrans “Tobelo 1” 8 0.133c 0.092c 0.225c
Myristica fragrans “Ternate 1” 0 0.190 cd 0.114bc 0.292bc
Myristica fragrans “Ternate 1” 4 0.264a–c 0.226ab 0.490ab
Myristica fragrans “Ternate 1” 8 0.284a–c 0.162bc 0.446ab

Numbers followed by the same letters in the same column did not differ significantly at p < 0.05 according to Duncanʼs multiple range test.

These results suggest that AMF inoculation on nutmeg cultivars elicits distinct physiological responses, particularly in leaf chlorophyll content. However, it is essential to note that different AMF doses are required for individual cultivars to increase the chlorophyll content in their leaves effectively.

5 K content of leaves

The application of AMF did not significantly interact with cultivars in determining the K content in leaves (Table 1). The leaf K content of nutmeg was very significantly (p < 0.01) determined by the cultivar and application of AMF dose (Table 1).

Table 4

Effect of cultivar and doses of AMF on K content of leaf at 28 WAI-P

K
%
Cultivars
Myristica fragrans ‘Makian’ 1.107b
Myristica fragrans ‘Tobelo 1’ 1.204a
Myristica fragrans ‘Ternate 1’ 1.055b
Doses of AMF (g seedling−1)
0 1.185a
4 1.106b
8 1.075b

Numbers followed by the same letters in the same column (varieties and doses of AMF) did not differ significantly at p < 0.05 according to Duncanʼs multiple range test.

Cultivar “Tobelo 1” exhibited the highest leaf K content (8.7–14.1%) and was significantly (p < 0.01) different from other cultivars. These results indicate that the leaf K content was genetically distinct. Meanwhile, without AMF inoculation, soil media produced the highest leaf K content (7.1–10.2%) and was significantly (p < 0.01) different from mycorrhizal AMF inoculation (Table 4). These results indicate that in the growing medium, the soil used for growing nutmeg provided an optimal supply of potassium (K) for the growth of nutmeg plants.

5.1 Growth

The application of AMF did not interact with cultivars in determining the LA, SDW, and RL. However, cultivars were very significant (p < 0.01) in determining LA, SDW, and RL (p < 0.05) (Table 1). Among the cultivars, “Ternate 1” produced the most extensive LA (36.7–106.9%) and SDW (27.8– 45.8%) that were significantly (p < 0.01) different from the other cultivars. In addition, “Ternate 1” demonstrated superior rooting properties, with a significantly (p < 0.05) longer RL (90.72%) compared to the “Makian” cultivar (Table 5).

Table 5

Effect of AMF and cultivars on the growth properties of nutmeg at 28 WAI-P

LA (cm2) SDW (g plant−1) RL (m)
Cultivars
Myristica fragrans “Makian” 636.0c 14.98c 4.969b
Myristica fragrans “Tobelo 1” 962.8b 21.64b 6.874ab
Myristica fragrans “Ternate 1” 1316.1a 27.66a 9.477a
Doses of AMF (g seedling −1 )
0 819.0b 19.482a 7.453a
4 1039.4a 23.369a 7.086a
8 1056.6a 21.439a 6.781a

Numbers followed by the same letters in the same columns (varieties and doses of AMF) did not differ significantly at p < 0.05 according to Duncanʼs multiple range test.

These results highlight the primary influence of genetic factors on growth traits, including LA, SDW, and RL. In contrast, the environmental factors and interactions with the growing media (AMF inoculation) appear to have less impact on these growth characteristics among the tested cultivars. The cultivar “Ternate 1” has exceptional traits and characteristics, including more prominent LA, higher SDW, and significant RL growth. These superior growth features make “Ternate 1” a standout cultivar in this study.

6 MR

Cultivar “Ternate 1” had a higher MR in the total plant biomass weight than the other cultivars (Figure 3). This finding indicates that the AMF inoculation treatment resulted in a more effective symbiosis in plant growth, increasing the plant biomass production.

Figure 3 MR to nutmeg cultivars at an AMF inoculation dose. (A) Cultivar “Makian” + 8 g AMF; (B) Cultivar “Makian” + 4 g AMF; (C) Cultivar “Tobelo 1” + 8 g AMF; (D) Cultivar “Tobelo 1” + 4 g AMF; (E) Cultivar “Ternate 1” + 8 g AMF; (F) Cultivar “Ternate 1” + 4 g AMF.
Figure 3

MR to nutmeg cultivars at an AMF inoculation dose. (A) Cultivar “Makian” + 8 g AMF; (B) Cultivar “Makian” + 4 g AMF; (C) Cultivar “Tobelo 1” + 8 g AMF; (D) Cultivar “Tobelo 1” + 4 g AMF; (E) Cultivar “Ternate 1” + 8 g AMF; (F) Cultivar “Ternate 1” + 4 g AMF.

Additionally, the highest MR observed in the “Ternate 1” cultivar can be attributed to its favorable growth genetic factors, including LA, SDW, and RL (Table 5). The combination of AMF inoculation with cultivar processing, such as growth genetic traits (Table 5), led to significant plant biomass weight compared to other cultivars (Figure 3). These results demonstrate that the high MR of a cultivar is influenced by its inherent genetic growth characteristics.

7 Agronomic traits that determine AM colonization

Agronomic traits, specifically Chl a, Chl b, and K content of leaves, were significant determinants of colonization in nutmeg plants. The influence of Chl a, Chl b, and K content of leaves strongly impacted the colonization ability (R 2 = 0.88) (Table 6). These findings highlight the crucial role of genetic traits, namely Chl a, Chl b, and K content of leaves, in determining the AM colonization ability of nutmeg cultivars.

Table 6

Summary of stepwise selection of agronomy traits on colonization

Agronomy traits Parameter estimate Standard error Type II SS F value Pr > F Model R-Square Pr > F
Chl a 22.247 4.336 47.58 26.32 <0.0001 0.787 <0.0001
Chl b −19.622 5.443 23.48 19.22 0.0014 0.849 0.0036
[K] in leaves 1.568 0.682 9.54 5.28 0.0306 0.876 0.0306
Sum of residuals = 0.6466 First-order autocorrelation = −0.0787
Sum of squared residuals = 41.435 Durbin-Watson D = 2.148
Sum of squared residuals = – Error SS -0.000 R-Square = 0.882

8 Discussion

Inoculation treatment of AMF significantly improved the colonization ability (p < 0.01) among the three cultivars. The range of AM colonization percentages of the three cultivars was 2.0–39.0%. Wide differences in percentage AM colonization among cultivars were also reported by De Vita et al. [44] on durum wheat (2.0–42.5%) and Yinan et al. [45] on chenopods (5–33%). Percentage AM colonization among cultivars was also reported by Elliot et al. [25] on wheat (56–87%) and by Wang et al. [46] on rice cultivars (28.1–57.9%).

This difference in AM colonization among nutmeg cultivars indicates the genetic characteristics. This is based on a report by De Vita et al. [44] that within a cultivar, there are differences in the ability to express genes associated with selection against AM symbiosis in quantitative trait loci (QTL). One of these QTL gene expressions plays an important role in host–parasite or disease/defense interactions. Besides, the percentage of AM colonization is also caused by differences in AMF species [44,47]. Meanwhile, the AMF inoculation applied contained a mixture of AMF species: Glomus sp., Funneliformis sp., Acaulospora sp., Gigaspora sp., and Scutellospora sp. Thus, these various AMF inoculations produce a wide range of percentage of AM colonization.

The AMF inoculation which increased the percentage of AM colonization subsequently significantly increased the chlorophyll content. The increase in Chl a (p < 0.05), Chl b (p < 0.01), and Chl (p < 0.01) was the result of AMF inoculum–cultivar interactions. The chlorophyll content among these cultivars was very significant. This means that there were differences in the AM colonization ability. The percentage of AM colonization is determined by genetic factor–gene expression [44] and the suitability of the host plant–AMF [48]. In fact, the colonization percentage of AM was strongly influenced (R 2 = 0.88) by Chl a, Chl b, and K content of leaves (Table 6). This result indicated that the cultivars provided higher leaf chlorophyll content due to the influence of AMF inoculation.

The application of 8 g seedling−1 of AMF dose on the cultivar “Makian” significantly increased Chl a, Chl b, and Chl. It also reached the highest level compared to other treatment combinations. This finding is in line with Chandrasekaran et al. [49] and Jabborova et al. [50] who state that mycorrhizal inoculation effectively increases leaf chlorophyll content.

High leaf chlorophyll levels at early growth in nutmeg are essential because it stimulates photosynthesis and plant growth [51,52]. Sulistiono et al. [17] and Mathur et al. [53] found that sugarcane and AMF-inoculated maize produced better leaf chlorophyll contents, resulting in a higher photosynthetic rate and better plant biomass. This suggests that there has been an increase in the cultivar biomass with AMF inoculation. This can be seen in the MR, which represents the benefit (if any) a plant gains from an AM fungal associate versus a non-mycorrhizal control [31,47].

The AMF inoculation at a dose of 4–8 g seedling−1 showed the most beneficial effect (MR) on cultivar “Ternate 1” with a biomass increase by 30–37.0%. The magnitude of MR depends on the combination of host plant species and AMF [48], timing, host plant growth, and form of carbon inputs into the soil [47]. In terms of host factors, it was found that the increase in MR was related to the percentage of AM colonization which was affected (R 2 = 0.88) by Chl a, Chl b, and K of leaves.

A higher percentage of AM colonization indicates a more optimal colonization process [54], where this process consists of (1) pre-infection, (2) penetration of the fungus to the roots, (3) formation of arbuscules and vesicle, (4) fungal elongation in the roots and rhizosphere, and (5) spread of fungi to the soil [55]. After optimum AM colonization, host–AMF symbiosis takes place. Arbuscules that have been formed help transport nutrients to plant cells, especially the P element [56]. The established photosynthate is used to form plant organs, thereby increasing the plant biomass (MR) [57,58].

The increase in the plant biomass observed in MR was caused by an increase in LA. This was based on AMF inoculation that significantly (p < 0.01) increased LA. LA increased at AMF inoculation (4–8 g seedling−1) by 26.9–29.0%, which is different from the control. These results are in line with previous findings by Liu et al. [59] that leaf growth in early stage is key to biomass. The increased LA will increase the rate of photosynthesis per unit LA [60]. The increased LA resulted in increase in the photosynthetic rate by increasing CO2 by 18–43% and increasing the photosynthetic rate by 48–85%. Both significantly affected the biomass production [61].

The results of this study indicate that the nutmeg cultivation system with AMF inoculation is necessary to increase LA. The AMF inoculation only increased the LA (p < 0.01) compared to the control apart from increasing Chl a, Chl b, and Chl. Cultivars “Makian” or “Ternate 1” can be prioritized for the selection of nutmeg cultivars for the development. This was due to the agronomic characteristics in the form of better Chl, which was significantly (p < 0.01) different from cultivar “Tobelo 1” (98–188%) with AMF inoculation at a dose of 8 g seedling−1.

Chl a and Chl b are crucial in sunlight absorption and photosynthesis [62,63]. This is because Chl a functions to capture the photosynthetic light of photosystems I and II (700 and 680 nm, respectively) to be converted into high energy such as ATP and NADP + H2. These high-energy sources are indispensable for carbon metabolism and growth [63].

Meanwhile, Chl b as an accessory pigment is not only a light-harvesting process and thermal energy dissipation but also a linear electron transport and repair process in grana [64]. Thus, the presence of Chl a and Chl b is the main determinant of the proportion of AM colonization. This is because the symbiosis between AMF and host plants is determined by photosynthesis [65].

Meanwhile, the K content of leaves has had less effect on the AM colonization because K content in leaves does not directly determine photosynthesis. K content regulates the osmotic balance of plant cells under salt stress, controls the opening of stomata, and helps plants adapt to drought stress [66,67]. Therefore, K leaves provide a determining influence on the proportion of AM colonization. This is consistent with a study by Jiang et al. [68] that the concentration of K leaf in bamboo seedlings was significantly affected by the inoculation of AM fungi.

Meanwhile, no application of AMF is necessary for AM colonization on soil with potential optimal AMF spores. Chen et al. [69] found that soil without mycorrhizal inoculation, such as pastures under long-term grazing, exhibited significantly increased spore density (12–28 spores g−1 soil) and hyphae length density (9–15 spores mg−1 soil). Similarly, in a small agroecosystem, soil fertility and vegetation are sources of diversity and density of the AMF [26]. In addition, non-sterile soil can suppress extra-radicals through a combination of abiotic factors such as rainfall and soil moisture, along with biotic factors such as certain bacteria and fungi, as highlighted by Svenningsen et al. [70] and Cruz-Paredes et al. [71]. This helps explain the occurrence of AM colonization in soil without AMF inoculation treatments.

9 Conclusions

The results of this study successfully addressed the research objective of developing a method to enhance the early growth of nutmeg. The application of AMF inoculation doses on specific cultivars proved effective in promoting the early growth of nutmeg. Notably, inoculation with 4–8 g of AMF per seedling increased the Chl a, Chl b, and Chl in the “Makian” and “Ternate 1” cultivars. The leaf chlorophyll content, an important agronomic trait, significantly influenced the percentage of AM colonization (R 2 = 0.88) and was determined by the Chl a, Chl b and K of the leaves. Specifically, inoculation of the cultivar “Makian” with 8 g of AMF per seedling showed the most significant increase in the total leaf chlorophyll (32.4–188.4%), which differed significantly from other cultivars. In addition, AMF inoculation resulted in increased AM colonization (2.0–39.0%), LA across cultivars (26.9–28.3%), and overall plant biomass, a determinant of MR. The cultivar “Ternate 1” showed the highest MR, indicating its potential for further development. Consequently, future studies should investigate the effects of AMF at the subsequent growth stages.

Abbreviations

AMF

arbuscular mycorrhizal fungi

Chl a

chlorophyll a

Chl b

chlorophyll b

LA

leaf area

MR

mycorrhizal response

SDW

shoot dry weight

Acknowledgments

The authors thank the nutmeg seed breeders in Ternate, Makian, and Tobelo of North Maluku Province, the nutmeg nursery technicians at IAAT North Maluku, technicians head of the Laboratory of Plant Science and Plant Pests and Diseases on UGM.

  1. Funding information: The authors state no funding involved.

  2. Author contributions: WS – conceptualization, methodology, formal analysis; writing – original draft, writing – reviewing and editing; HBA – prepared research material, collected data; SH – methodology, original draft, writing–reviewing and editing; JAL – prepared research material, collected data; SS – methodology, reviewing and editing; YA – conceptualization, writing–reviewing and editing; MR – reviewing and editing.

  3. Conflict of interest: The authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2023-02-06
Revised: 2023-07-20
Accepted: 2023-07-21
Published Online: 2023-08-29

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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https://doi.org/10.1515/opag-2022-0215
Keywords for this article
AMF inoculation; biomass; chlorophyll; growth; nutmeg cultivars; root colonization
Creative Commons
BY 4.0

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  72. In vitro and in silico study for plant growth promotion potential of indigenous Ochrobactrum ciceri and Bacillus australimaris
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