12
Journal of PhytoPathology and Disease Management
Print ISSN: 3009-6111 Online ISSN: 3009-6170
Volume 11, Issue 1, 2024, Pages 1218
Review Article
Integrated management strategies for septoria leaf spot in pistachio
(Pistacia vera): Challenges and advances
Abdelhak Rhouma1 | Rabeb Rhouma2 | Lobna Hajji-Hed1 | Okon Godwin Okon3 | Pravin Babasaheb Khaire4
1Research Laboratory of Agricultural Production Systems and Sustainable Development LR03AGR02, Regional Centre of Agricultural
Research of Sidi Bouzid, CRRA, Gafsa Road Km 6, B.P. 357, Sidi Bouzid, 9100, Tunisia
2École nationale d’ingénieurs de Sfax, Tunisia
3Department of Botany, Akwa Ibom State University, Ikot Akpaden 532111, Nigeria
4Department of Plant Pathology and Microbiology, Mahatma Phule Krishi Vidyapeeth, Rahuri 413722 Maharashtra, India
DOI:
10.5281/zenodo.14511057
ARK:
ark:/24629/PPDJ.v11i1.254
Received:
8 November 2024
Accepted:
25 November 2024
Published online:
28 November 2024
Correspondence:
Abdelhak Rhouma
Research Laboratory of Agricultural
Production Systems and Sustainable
Development LR03AGR02, Regional
Centre of Agricultural Research of
Sidi Bouzid, CRRA, Gafsa Road Km 6,
B.P. 357, Sidi Bouzid, 9100, Tunisia.
Email: abdelhak.rhouma@gmail.com
Abstract:
Pistachios are economically important crops facing increasing threats from fungal
diseases, particularly Septoria leaf spot, which has a significant global impact, causing
substantial yield losses and economic damage worldwide. This review comprehensively
examined existing literature on Septoria leaf spot of pistachio, including peer-reviewed
articles, scientific reports, and relevant databases, to characterize the disease, assess its
impact on pistachio production, and evaluate available management strategies. Septoria
leaf spot is a significant foliar disease causing severe defoliation and yield reduction,
prevalent in major pistachio-growing regions. Management strategies reviewed include
cultural practices (proper irrigation, sanitation, and weed control), biological control
(utilizing beneficial microorganisms), chemical control (employing fungicides
strategically), and host resistance (utilizing resistant cultivars). Effective management
requires an integrated approach combining multiple strategies, with continued research
crucial to develop novel and sustainable control methods, such as improved fungicides
and the identification and utilization of highly resistant cultivars. Implementing these
strategies will enhance pistachio tree health, improve yield and quality, and ensure the
long-term sustainability of pistachio production.
Keywords:
Management practices, Pistacia vera, Septoria spp., sustainability.
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13 | Journal of Plant Pathology and Disease Management | Vol. 11, No. 1 |
1. Introduction
Within the genus Pistacia of the family Anacardiaceae, only
the Pistacia vera L. bears edible nuts (FAOSTAT, 2017; Gusella
et al., 2022). Pistachio nuts have recorded a tremendous
increase in global production (Mir-Makhamad et al., 2022).
The wild type is native to western Asia and Asia Minor and
found in parts of Africa, southern Europe, Turkey, Syria, Iran,
Iraq, India, Lebanon, and Palestine (Mandalari et al., 2022).
Pistachios belong to the category of drupes as classied by
botanists. They thrive under long, hot summers and mild
winters with at least 1000 hours below 7.2°C (Batovska and
Inbar, 2024). They do well in various types of soils: saline,
alkaline, ne sandy loams, and those high in lime (Benny et
al., 2022). The recent discovery of new and existing pistachio
diseases has reduced the yield and quality of fruit
considerably. This emergence could be attributed to several
factors, such as increased understanding of disease-causing
agents, innovation in agricultural practices, and expansion of
pistachio culture into diverse geographic regions under
varying ecological conditions. Such changes must have
inuenced the prevalence and dissemination of certain
pistachio diseases. Of these, Septoria Leaf Spot is considered
to pose a serious threat both to yield and fruit quality. To this
date, control of fungal infections has traditionally been
carried out by the application of chemical fungicides. In
recent times, however, interest has grown in more
environmentally friendly control strategies, among which
biological control measures are right at the forefront.
Septoria leaf spot is a fungal disease aecting pistachio trees,
primarily in Mediterranean climates. Caused by various
Septoria species, it manifests as brown spots on leaves that
can enlarge, leading to leaf drop and reduced fruit quality.
The fungus overwinters on fallen leaves, and spores spread
through wind and rain (Avenot et al., 2016; Guldur et al., 2011;
López-Moral et al., 2022; Nazarova et al., 2023; Ozkiling &
Kurt, 2017). The aim of this review was to discuss
methodologies that may be used for the management of such
harmful infections through various strategies. Further
discussion will emphasize the virulence factors employed by
these fungi in the process of pistachio infection and
developing the disease. This review will also critically analyze
the existing control methods, including chemical fungicides,
cultural controls, and newer approaches involving biological
control agents. The review is intended to present an overview
of the pathogenicity of these fungal infections and assess
various methods of management in pistachio production.
2. Septoria leaf spot of pistachio
2.1 Symptoms
The disease rst appears as small, circular, or irregularly
shaped necrotic areas belonging to dead tissues on either side
of the leaf surface. They are usually conned within small
veins, have small dimensions of about 1-2 mm in diameter,
and with time keep the size small and sometimes even
discrete by showing slow increase in size (Nazarova et al.,
2023). In highly diseased leaves, hundreds of such spots may
appear on them. As the disease progresses, larger sections of
the leaf tissue turn brown (López-Moral et al., 2022). This
often results in large infections causing early defoliation that
reduces the photosynthetic capacity of the tree. That then
leads to reduced carbohydrate production and storage of
carbohydrates, and thus the general vigor and health of the
tree decline (Figure 1) (Teviotdale et al., 2002).
2.2 Disease cycle
Overwintering of the fungal pathogen occurs in already
infected leaves that fall on the orchard oor. These leaves
serve as a reservoir for the pathogen during the winter
months. During this stage, the fungus resides in a type of
specialized structure called pycnidia, which is a spore-
producing body. In the spring, after precipitation events such
as rain or irrigation, pycnidia release the spores of the fungus.
Wind or water droplets, thus facilitating their transmission
to new, susceptible leaves, thereby initiating new infection
cycles (Figure 2), can then disperse the spores (Chitzanidis,
1956; Eskalen et al., 2001; Gusella et al., 2021).
2.3 Conditions for disease
Septoria pistaciarum, the fungal agent of Septoria leaf spot,
exhibits a distinct host range and overwintering habit. Thus,
this pathogen infects only pistachio trees (Crous et al., 2013).
At the close of any growing season, leaves of diseased trees
infected with the fungus from the previous year fall to the
ground. The diseased leaves serve as a reservoir for the
pathogen to survive the winter months (Nazarova et al.,
2023). Specialized fruiting structures, called pycnidia, form
within the fallen, infected leaves in late winter and early
spring. The pycnidia serves as spore-producing bodies,
carrying the fungal spores that initiate new infections. With
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14 | Journal of Plant Pathology and Disease Management | Vol. 11, No. 1 |
rainfall, spores are liberated from the pycnidia (Eskalen et al.,
2001). Rain and wind help in the spread of spores toward
healthy pistachio leaves. The spores can germinate and then
directly penetrate the leaves to establish new infections and
perpetuate the disease cycle upon landing on susceptible leaf
tissue (Crous et al., 2013).
Figure 1: Septoria pistaciarum is a causative agent of pistachio leaf spot. a. Field symptoms (June); b.
Leaf spot details; c. Crystalline cirrus exuding from a lesion; d. End-of-July symptoms (coalesced lesions
resulting in necrotic patches); e. Senescent fallen leaf symptoms (November); f. Isolation results
showing constant presence of the same Septoria-like colony (Gusella et al., 2021; Gusella et al., 2022).
Figure 2: Cycle of Septoria pistaciarum. Seasons details, perithecium with asci (a) and pycnidium with
pycnidiospores (b) (Chitzanidis, 1956; Gusella et al., 2021; Gusella et al., 2022).
Review Article | Alsaiari et al.
15 | Journal of Plant Pathology and Disease Management | Vol. 11, No. 1 |
2.4 Management approaches
The literature indicates a lack of substantial scientic
research and published data specically on this plant disease
aecting pistachio trees. This scarcity could stem from
limited research conducted, limited publication of existing
ndings, or the dispersion of information across various
sources. This limited information poses signicant
challenges, including diculties in managing the disease
eectively for growers due to insucient guidance, limited
understanding of the disease's underlying causes hindering
the development of eective control measures, and obstacles
for researchers in building upon existing knowledge due to
the limited availability of reliable data (López-Moral et al.,
2022; Nazarova et al., 2023). The management of Septoria leaf
spot in orchards requires an integrated approach. The basis
of this is good sanitation practice. This approach directly
targets the inoculums, those infective propagules responsible
for the next growing season. They include raking and
destroying fallen leaves, pruning dead and dying branches,
and removing weeds within and surrounding the orchard
area. This sanitation practice removes the inoculum
harbored in host plant materials over winter, thereby
reducing by a great magnitude the inoculum levels that
would have otherwise been available to initiate new
infections the following spring (Drais et al., 2023). Where S.
pistaciarum has been identied to be an existing problem in
pistachio orchards, preventive fungicide applications may be
a complementary control measure. Predictive timing of the
fungicide application is crucial for eective disease
management. Applications must be conducted based on
predictive models or when environmental conditions are
identied that signal favorability for the disease
development, such as frequent rain or high humidity. This
targeted approach will limit the rate of fungicide application
to the appropriate amount, thus contributing to maximizing
eciency in the control of fungal diseases (Sarpkaya, 2014).
A few fungicides with dierent modes of action are registered
for managing Septoria leaf spot in pistachio orchards.
Azoxystrobin and trioxystrobin are classes of strobilurin
fungicides. Both interfere with the fungal respiratory chain
by disrupting the production of the high-energy electron
carriers within the pathogen. Copper hydroxide interferes
with the fungal cell membrane and protein synthesis due to
its non-specic mode of action. Potassium bicarbonate
interferes with fungal growth by changing cellular pH and
oering uninhabitable environments. Chlorothalonil
inhibits all types of metabolic processes in the fungal
pathogens, thus impeding their growth and ability to infect
plant tissues (Luo et al., 2007). In this vein, if pistachio
growers were allowed to practice good sanitation and apply
fungicides as targeted applications when the environmental
conditions favored the development of the disease, this
would manage the disease Septoria leaf spot and, by such
consideration, protect health in crops (Çat, 2022). Limited
commercial pistachio cultivars with host resistance
necessitate the exploration of alternative strategies for
inducing systemic acquired resistance (SAR). Synthetic,
natural, and peptide-based compounds are being
investigated for the management of Septoria leaf spot. Κ-
carrageenan, a sulfated polysaccharide derived from
Kappaphycus alvarezii (marine red seaweed), has
demonstrated SAR induction in susceptible tomato cultivars,
enhancing their tolerance to infection by Solanum lycopersici
(Mani et al. 2021). Furthermore, many study evaluated the
ecacy of botanicals traditionally used in indigenous
technical knowledge for plant disease control (Hajji-Hed et
al., 2024a; Hajji-Hed et al., 2024b; Matrood and Rhouma,
2021). Biological control agents (BCAs) are favored by some
growers due to their generally high toxicological safety prole
and reduced environmental impact compared to
conventional chemical pesticides. These agents have been
successfully employed in the management of various plant
diseases. For example, the application of Metarhizium spp.
and Beauveria bassiana to seedlings has demonstrated
signicant ecacy in suppressing several soilborne diseases,
including Damping-O, Root Rot, and Fusarium wilt
(Rhouma et al., 2024a; Rhouma et al., 2024b). Additionally,
Trichoderma spp. and Pseudomonas spp., which are also
recognized as prominent BCAs, have proven eective in
controlling gray mold disease (Hajji-Hed et al., 2023).
3. Conclusion
Septoria leaf spot in pistachio necessitates the development
and implementation of innovative disease management
strategies beyond traditional fungicides. Short-term eorts
should focus on optimizing existing technologies through
rened integrated pest management (IPM) approaches. This
includes incorporating biological control agents,
implementing cultural control measures, and judiciously
utilizing fungicides. Simultaneously, research eorts should
Review Article | Alsaiari et al.
16 | Journal of Plant Pathology and Disease Management | Vol. 11, No. 1 |
prioritize developing ecient and accessible methods for
phenotyping Septoria leaf spot resistance and expanding the
search for resistant germplasm. To overcome current
limitations in developing durable resistance, mid-term
strategies should emphasize the application of advanced
plant breeding technologies, such as CRISPR-Cas9 and
genomic selection. Collaborative research initiatives are
crucial to enhance our understanding of host-pathogen
interactions, identify novel resistance mechanisms, and
develop eective disease management strategies for a broader
range of diseases and abiotic stresses. The long-term
objective is to fully integrate durable resistance into pistachio
production systems. This requires the establishment of
robust and adaptable IPM frameworks that combine
biological, botanical, and sustainable agronomic practices
with host resistance. Continuous monitoring and
adjustments of these systems are essential to address the
evolving challenges posed by pathogen populations,
environmental stresses, and climate change. The successful
implementation of these strategies will require the
development of predictive models and the integration of
articial intelligence-driven decision-making tools. A
multidisciplinary approach that prioritizes ecological
sustainability, farmer engagement, and scientic innovation
is crucial for eective Septoria leaf spot management and the
long-term sustainability of the pistachio industry.
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Acknowledgments: Authors are thankful to the review
editor and anonymous reviewers for their invaluable
comments and suggestions for improving the clarity of the
research paper.
Funding Information: The authors received no external
funding for this article.
Data Availability: Data are available upon request.
Correspondence and requests for materials should be
directed to Abdelhak Rhouma .
Author Contributions: All authors contributed equally to
this work and share rst authorship.
Human and Animal Rights: This research did not involve
human or animal subjects.
Conicts of Interest: The authors report no known
nancial or personal relationships that could have inuenced
the work presented in this article.
How to cite this article: Rhouma, A., Rhouma, R., Hajji-
Hed, L., Okon, O.G, & Khaire, P.B. (2024). Integrated
management strategies for septoria leaf spot in pistachio
(Pistacia vera): Challenges and advances. Journal of
PhytoPathology and Disease Management, 11(1), 1218.