1. Introduction
Mangoes are the main horticultural crop of the Northern Territory (NT), the largest producer of mangoes in Australia. NT growers produce 52% of the nation's mangoes and give Australian customers their first crop harvest of the season. The mango industry provides approximately
$128 million to the NT economy and employs about 3500 people [
1]. However, plant diseases pose a significant threat to maintaining or increasing mango production in the NT. Plant diseases can significantly reduce farm profitability owing to yield losses, higher production costs, and poorer crop quality [
2,
3,
4]. Some of the common mango diseases in the NT include anthracnose [
5], stem end rot [
2,
6], resin canal discoloration [
3,
7], and sudden decline or common dieback [
8,
9,
10].
Common dieback causes serious production issues for mango growers [
8,
9,
10,
11,
12,
13,
14]. It is characterized by a progressive and downward drying out or dying back of the twig or branch, sometimes with the death of the whole branch. Twig/branch/stem cankers are also a typical symptom. In very severe cases, this dieback can lead to the death of the mango tree, particularly when trees are under prolonged periods of drought with inadequate irrigation. Tree death is not common in managed orchards. Common die-back symptoms are not frequently found on young trees, its intensity appears to in-crease with the plant age [
14]. Some visible symptoms of common dieback include gummosis, vascular discoloration, death of twigs from the top, streaking, and bark splitting. The leaves of the affected tree dry up and remain attached to the dying tree, and the infected trunk oozes badly with a smelling exudate [
10,
11,
12]. Both biotic and abiotic factors are likely to be responsible for the symptoms of mango dieback. For biotic factors, reports identified several genera and species in the family Botryosphaeriaceae as organisms associated with dieback in mangoes [
8,
10]. Moreover, abiotic factors that may play a role in dieback include relative humidity, high temperatures, sun scald, water stress, drought, and cultural management practices [
11,
13].
Mango growers in the Darwin region of NT reported a type of dieback that showed different symptoms compared with that of common dieback. The symptom was a dark longitudinal lesion that was only on one side of the last twig flush above the last node. The apical bud dies as the lesion spreads upward and downward. The leaves of the last flush dried out and temporarily stayed affixed to the twig. Occasionally, only the apical bud had dried leaves on one side, and a black lesion was visible on the second and third flushes, with or without gum exudation. The middle of the twig, either between two nodes or between the apical bud and terminal node, appears to be where the majority of lesions are located. Moreover, the internal lesion extended a few centimeters beyond the visible symptoms. Transversely cutting the twig reveals that the lesion is not in the center but on the outside. Thus, it is called twig-tip dieback (MTTD), which distinguishes it from common dieback (
Figure 1). The etiology of MTTD, if biotic or abiotic, is presently unknown. The intensity of MTTD differed among orchards, with certain locations experiencing severe impacts. MTTD severity varied across orchards, impacting some areas more severely than others. MTTD occurrence was not solely dependent on plant stress, as it had been found in orchards with healthy trees and even in previously abandoned settings. Remarkably, MTTD affected young mango trees, particularly the KP cultivar, showing its susceptibility regardless of tree age [
15].
Mineral nutrition is important not only for the optimum growth and yield of mangoes but also plays a significant role in plant and disease interactions [
16,
17]. The nutrient composition and imbalances affect plant growth, flowering traits, fruit development [
18], and disease susceptibility through metabolic changes that influence the vascular system of plants [
10,
19,
20]. Adequate levels of essential nutrients are also needed for key physiological processes such as photosynthesis and stomatal regulation, which determine how trees cope with stress [
21]. Furthermore, because of the direct role of mineral elements in plant defense, comprehensive and balanced nutrition has traditionally been the first line of defense for plants by modifying root exudates, the dynamics of the microflora population, and the production of phytoalexins, all of which have a direct impact on plant health [
16]. Thus, ensuring comprehensive and balanced nutrition stands as the cornerstone of safeguarding plant health, highlighting its pivotal role as the primary defense mechanism for plants against adversity and disease challenges.
However, there are no reports on the effect of MTTD on mineral nutrition in mangoes. In common dieback, studies have shown that nutrient stress predisposes and contributes to the common dieback problem in sugar maples [
22], cherries [
23], eucalypts [
24], and other trees [
25]. Saeed et al. [
11] found that common dieback disturbs the level of important phytochemicals and minerals in the stem bark of mango. In citrus, the effects of Huanglongbing (HLB) pathogen infection on P resorption efficiency (PRE) varied depending on the species of citrus [
26]. Therefore, it is important to elucidate the effects of MTTD on the nutrient dynamics and resorption efficiency (RE) of mangoes. Because leaves are the most dynamic and responsive plant part for metabolic activity and nutrient availability [
27], leaf nutrient analysis provides the actual uptake of nutrients and indicates the existing nutrient levels when compared to the standard optimum leaf nutrient content [
28]. Leaf analysis can identify imbalances and aid in formulating fertilizer recommendations to address nutritional deficiencies [
16]. Moreover, nutrient analysis of senescing leaf samples provides information on the nutrient resorption efficiency [
29].
The investigation into the cause of MTTD is ongoing. In this study, we present the analysis of nutrient levels in a commercial mango orchard featuring trees exhibiting varying degrees of MTTD. This study aimed to (1) assess leaf nutrient levels in trees affected by differing MTTD intensities, (2) ascertain if MTTD intensity contributes to elevated nutrient imbalances, and (3) understand how MTTD intensity influences the nutrient resorption efficiency of mango trees.
4. Discussion
Plant disease management is a major concern for mango growers, and knowledge about the interplay between mineral nutrition and plant diseases is indispensable for effective crop management and promoting sustainability in agriculture moving forward. Both plants and pathogens require mineral nutrients, which play a significant role in their interactions [
16,
42]. This pilot study focuses on understanding the influence of MTTD on the mineral nutrition of mango. We found that there was no relationship between soil nutrients and MTTD severity, but leaf nutrient contents varied significantly between LD and HD trees (
Table 1,
Figure 4). The result indicates a direct and significant impact on the nutrient content of tree leaves, independent of soil nutrient availability, as all trees may have similar opportunities for accessing nutrients from the soil and applied fertilizer. In oak tree decline, Azim Nejad et al. [
43] also reported that the physical and chemical properties of soil are not determinant factors. Moreover, there were no significant differences in the soil properties of samples collected from healthy trees and those infected with HLB, thus, it is unlikely that the difference in foliar mineral concentrations between infected and PCR-negative trees was due to the differences in soil [
44].
The findings also demonstrated that MTTD severity significantly alters several nutrients levels, while others remain at comparatively constant amounts, regardless of the severity of MTTD (
Figure 4). This result indicates that the impact of MTTD is nutrient-specific. It also corroborates a study showing the variable effects of diseases on the nutrient content of citrus [
36], coconut palm [
45], and cacao [
46]. For example, in Valencia orange, the severity of the citrus decline index is negatively correlated with Ca, Mg, S, and B and positively correlated with high leaf N, P, K, Cu, and Mn indices in the leaves [
36]. Moreover, healthy coconut palms had higher macronutrient (N, P, K, Ca, Mg, and S) and micronutrient (B and Cu) uptake than those with root wilt disease trees, while Mn and Zn were comparable between healthy and diseased trees [
45]. In cacao, leaves infected with witches’ broom disease caused by
Monoliophtora perniciosa had lower Ca, Mg, S, Fe, and Mn contents in healthy leaves than diseased leaves. Moreover, P and Cu contents were higher in diseased leaves than in healthy leaves, but N, K, and Zn were comparable between healthy leaves and leaves of vegetative broom, indicating differential changes in the concentration of nutrients in the presence of
M. perniciosa infection [
46].
The increase in K in the leaves of HD trees (
Figure 4 and
Figure 5) is in line with the report of Putiska et al. [
44], showing that a significant negative relationship (r = -0.71) existed between the symptom severity of HLB and concentrations of K in Siem mandarin (
Citrus reticulata) in Indonesia. Spann and Schumann [
42] also observed an elevated concentration of potassium (K) in citrus (
C. sinensis) infected with HLB in three out of four orchards. They attributed this increase to the diminished growth of the trees and an apparent concentration of K induced by HLB. Furthermore, the findings in this study, where HD trees exhibited high K and low Ca leaf contents, suggest a negative interaction between these nutrients. This interaction could be explained by the competition for the same absorption sites in the plant [
47]. Maintaining a balanced level of Ca and K has been shown to reduce the severity of disease and defoliation caused by the fungus
Calonectria pteridis in eucalyptus plants. The elevation in K levels may have contributed to a decrease in the stomatal closure response and an increase in stomatal opening movement, potentially facilitating infection by the pathogen. Under insufficient Ca concentration, substances such as sugars and amino acids may leak into the apoplast, providing the pathogen with resources for its growth and development [
47,
48,
49].
Our study showed that HD trees experienced more pronounced nutrient imbalances (
Figure 5), which may have predisposed the plants to disease susceptibility. Studies have shown that orchards with higher nutrient imbalance indices recorded higher disease severity [
15,
36,
47,
50]. The specific nutrient imbalances observed in HD trees may have implications for their health and growth, highlighting the importance of integrated nutrient and disease management strategies in mango production to address these imbalances and promote tree health. The emphasis on balanced nutrition as the first line of defence against diseases in crops stresses the significance of providing plants with the necessary nutrients to increase their natural defences. It is a preventive measure that supports plant health, resilience, and sustainable crop management strategies [
16,
51]. According to Tadayon and Sadeghi [
36], balanced nutrition management could reduce the severity of citrus decline in Valencia orange orchards by increasing the leaf concentrations of Ca, B, S and Mg as higher concentrations of these nutrients were positively correlated with a lower citrus decline severity index. In our earlier report, we found that the imbalance of nutrients such as Ca/Cu, B/Mn, and Fe/Zn ratios may have contributed to the development of RCD mango, a quality defect that appears during fruit ripening, reduces the market price and consumer appeal of mango fruits [
7].
This study showed that MTTD significantly reduced the nutrient RE of macronutrients N, P, and S and micronutrients Cu, Fe, and Zn in dieback affected leaves (
Figure 6). However, MTTD infection increased the resorption efficiency of K but did not affect Ca, Mg, and Mn, indicating that MTTD influences most of the mobile elements and less of the immobile elements. According to reports, Ca and Mn have poor mobility in the phloem sap, while N, P, K, S, Cu, Fe, and Zn are mobile elements [
52,
53,
54]. Though not as low as that of Ca, Mg transport is likewise low in both xylem and phloem [
52,
55]. A high concentration of nutrients in leaves coupled with low nutrient resorption typically indicates a strategy where plants invest resources extensively for rapid growth and development. Conversely, a low concentration of nutrients in leaves along with high nutrient resorption signifies a strategy where plants conserve nutrients, prioritizing survival and reproduction over immediate growth [
40]. Moreover, the increase in KRE in this study could be explained by the increase in K concentration in the leaves as affected by MTTD infection (
Figure 4). The reduction in nutrient resorption efficiency would also mean that plants would have to increase their nutrient intake from the soil, which would be more costly in low-nutrient environments [
38]. This is detrimental to the nutritional economics of trees because it can shorten leaf lifetime, limit photosynthetic capacity, and lessen internal nutrient cycling [
56]. Furthermore, the current season's slower growth will have a cumulative effect on the upcoming years as nutrient reserves in perennial tissues are depleted [
57]. Boercher [
58] reported that infection of
Arabidopsis thaliana leaves with
Pseudomonas syringae significantly reduced nutrient remobilization, which resulted in a significant fitness cost. In citrus, the effects of HLB pathogen infection on PRE varied depending on the species of citrus, such that HLB increased PRE in
Citrus limon. In contrast, HLB had no significant effect on
C. maxima species and substantially decreased in HLB-infected
Citrus reticulata, which may account for the marked decrease in average fruit yield [
25].
Overall, information on the nutrient-disease interaction is important owing to the various roles of nutrients in disease management, including forming robust cell walls, generating natural defense compounds like phytoalexins and antioxidants, fostering flavonoid production, and activating enzymes involved in phenol and lignin synthesis [
16,
51,
59]. N stands as a vital element for mango trees, crucial in improving vigor, promoting vegetative growth, and supporting physiological development. P plays a pivotal role in cell division, developmental processes, and the creation of sugar phosphate molecules, while K aids in pathogen and insect resistance, regulating water uptake, and influencing the quality of fruits. Ca contributes to membrane stability and reinforces cell walls. It also holds particular significance during the initial growth stages following mango harvesting, preserving fruit firmness. Mg is indispensable for chlorophyll production, while S supports enzymatic functions and protein synthesis [
15,
52,
60]. Micronutrients such as B, Cu, Fe, Mn, and Zn are crucial for overall plant health. Fe and Mn aid in chlorophyll synthesis, and Zn plays a key role in protein formation and regulating water movement in mango plants. Moreover, B facilitates cell division, ensuring effective pollination and fruit development, while Cu is vital for photosynthesis by lignifying cell walls to enable efficient carbohydrate and water transport within the plant [
15,
52,
60,
61].