Multi-scale defense architecture in sorghum: Canopy geometry, midrib fortresses, and information-aligned immune portfolios for ecological resilience

Multi-scale defense architecture in sorghum: Canopy geometry, midrib fortresses, and information-aligned immune portfolios for ecological resilience | Authorea try { document.documentElement.classList.add('js'); } catch (e) { } var _gaq = _gaq || []; _gaq.push(['_setAccount', 'G-8VDV14Y67G']); _gaq.push(['_trackPageview']); (function() { var ga = document.createElement('script'); ga.type = 'text/javascript'; ga.async = true; ga.src = ('https:' == document.location.protocol ? 'https://ssl' : 'http://www') + '.google-analytics.com/ga.js'; var s = document.getElementsByTagName('script')[0]; s.parentNode.insertBefore(ga, s); })(); Skip to main content Preprints Collections Wiley Open Research IET Open Research Ecological Society of Japan All Collections About About Authorea FAQs Contact Us Quick Search anywhere Search for preprint articles, keywords, etc. Search Search ADVANCED SEARCH SCROLL This is a preprint and has not been peer reviewed. Data may be preliminary. 3 December 2025 V1 Latest version Share on Multi-scale defense architecture in sorghum: Canopy geometry, midrib fortresses, and information-aligned immune portfolios for ecological resilience Authors : Eze Ahn 0000-0003-4447-4104 [email protected] , Insuck Baek , Louis K. Prom , Seunghyun Lim , Sunchung Park 0000-0002-7398-9476 , Moon S. Kim , Lyndel W. Meinhardt , and Clint Magill Authors Info & Affiliations https://doi.org/10.22541/au.176477982.26936740/v1 293 views 150 downloads Contents Abstract Supplementary Material Information & Authors Metrics & Citations View Options References Figures Tables Media Share Abstract This study unifies canopy geometry, tissue-specific resistance, and information-theoretic defense portfolios in sorghum challenged by Colletotrichum sublineola . We demonstrate that drooping canopies, midrib ”fortresses,” and information-aligned immune allocation jointly constitute a multi-scale defense architecture that enhances ecological resilience against anthracnose epidemics. Multi-scale defense architecture in sorghum: Canopy geometry, midrib fortresses, and information-aligned immune portfolios for ecological resilience Ezekiel Ahn 1,* , Insuck Baek 2 , Louis K. Prom 3 , Seunghyun Lim 1 , Sunchung Park 1 , Moon S. Kim 2 , Lyndel W. Meinhardt 1 , Clint Magill 4 1 Sustainable Perennial Crops Laboratory, Agricultural Research Service, United States, Department of Agriculture, Beltsville, MD, 20705, USA 2 Environmental Microbial and Food Safety Laboratory, Agricultural Research Service, United States, Department of Agriculture, Beltsville, MD, 20705, USA 3 Insect Control and Cotton Disease Research, Agricultural Research Service, Southern Plains Agricultural Research Center, United States Department of Agriculture, College Station, TX, 77845, USA 4 Department of Plant Pathology and Microbiology, Texas A&M University, College Station, TX, 77843, USA * Author to whom correspondence should be addressed (email: [email protected] ). Summary statement This study unifies canopy geometry, tissue-specific resistance, and information-theoretic defense portfolios in sorghum challenged by Colletotrichum sublineola . We demonstrate that drooping canopies, midrib ”fortresses,” and information-aligned immune allocation jointly constitute a multi-scale defense architecture that enhances ecological resilience against anthracnose epidemics. Keywords Sorghum anthracnose; Canopy architecture; Midrib defense; Defense portfolio Main Sorghum anthracnose, caused by Colletotrichum sublineola , remains a critical constraint on production, with epidemics modulated by both pathogen diversity and host architecture. While classical studies have linked canopy geometry to disease avoidance (Ahn, Odvody, Prom & Magill 2020), and tissue-specific responses to resistance (Ahn, Prom, Odvody & Magill 2018, 2019), it remains unclear how these structural and molecular layers integrate into a coherent defense strategy. Bridging these scales is particularly urgent under changing climate regimes, where altered rainfall patterns may reshape the physics of splash dispersal (Falster & Westoby 2003). Here, we propose a ”defense architecture” framework that quantifies how plants allocate structural and molecular assets to manage epidemiological risk. Detailed experimental protocols and statistical models are provided in the Supporting Information (Methods S1). We re-analyzed extensive greenhouse and excised-leaf datasets for sorghum ( Sorghum bicolor ) and its wild relative johnsongrass ( S. halepense ), a known pathogen reservoir. First, we characterized the ”leaf angle morphospace” using Principal Component Analysis (PCA) of 8-leaf profiles, revealing a structural continuum from erect sorghum to drooping johnsongrass (Fig. S1). Genotype-specific architectural traits are summarized in Table S1. Correlation analysis confirmed that architectural traits, particularly the slope of leaf angle distribution, were strong predictors of disease severity, whereas simple mean angles showed weaker associations (Fig. S2). To quantify this, we defined a structural defense index,\(\lambda_{\text{arch}}=-\ln\left(P_{severe,GH}\right)\). A simple linear model using mean angle and angle slope explained S3). Crucially, extending this to a non-linear ”canopy funneling” model incorporating the squared slope term increased explanatory power to droop slopes effectively shed inoculum, creating an emergent structural defense predictable from simple geometric traits. This structural layer serves as the first line of defense against splash-dispersed pathogens. In contrast, johnsongrass genotypes combined both strong canopy funneling and strong midrib protection, consistent with its role as a persistent pathogen reservoir that must tolerate repeated infection cycles while maintaining vigor (Xavier, Mizubuti, Queiroz, Chopra & Vaillancourt 2018; Pagán & García-Arenal 2020; Ahn, Prom & Magill 2021). Figure 1 Multi-scale defense architecture in sorghum: From canopy physics to information portfolios. (A) Canopy scale: A non-linear ”canopy funneling” model (dashed line) relates the canopy droop slope (angle vs. leaf position) to mean greenhouse anthracnose severity. The model explains ~87% of the variance (\(R^{2}\approx 0.87\)), indicating that genotypes with steeper droop slopes (right side) effectively shed inoculum, creating a physical barrier to infection. (B) Tissue Scale: The ”midrib fortress” effect. Paired bar chart showing the probability of severe infection (\(P_{\text{severe}}\)) for leaf blades (blue) versus midribs (orange) across four representative genotypes. The protection index (\(\Delta P=P_{\text{leaf}}-P_{\text{midrib}}\)) quantifies the reduced susceptibility of the vascular midrib compared to the lamina. Note that midrib protection persists even in the susceptible genotype BTx623 (\(\Delta\text{P\ }\approx 0.11\)). (C) Information scale: The defense portfolio map. Genotypes are plotted based on their portfolio risk (X-axis: Jensen-Shannon Divergence, representing the mismatch between attack patterns and defense allocation) and defense return (Y-axis: Overall protection probability,\(\ 1-P_{\text{avg}}\)). The marker color represents the structural defense index (\(\lambda_{\text{arch}}\)), derived from canopy geometry (imputed for missing values). The dashed line indicates the empirical ”efficient frontier.” The resistant line SC748-5 (low risk, high return) and the reservoir host SH1350 (high structural defense) exemplify distinct, optimized strategies, whereas BTx623 (high risk, low structural defense) exhibits a systemic resilience deficit. At the tissue scale, excised-leaf assays revealed a consistent ”midrib fortress” effect across genotypes. Midribs exhibited significantly lower susceptibility than adjacent leaf blades, quantified by a protection index \(\Delta P=P_{\text{leaf}}-P_{\text{midrib}}\) (Fig. 1B). Detailed severity probabilities for each genotype confirmed that this fortification was evident even in susceptible genotypes like BTx623 (\(\Delta\text{P\ }\approx 0.11\); Data S1), suggesting that vascular protection is a conserved, basal strategy decoupled from canopy geometry. To evaluate the efficiency of these defenses, we applied an information-theoretic approach. Using qPCR data (Table S2), we constructed a ”defense allocation distribution” (Q) and compared it to the empirical ”attack distribution” (P). The mismatch was quantified using the Jensen–Shannon Divergence (JSD). Mapping genotypes onto a ”defense portfolio” plane (Risk = JSD, Return = Overall Protection) revealed striking strategic divergences (Fig. 1C). The resistant line SC748-5 occupied an efficient frontier, allocating immune resources precisely where attacks occurred (\(\text{JSD\ }\approx 0\)). In contrast, the susceptible BTx623 exhibited a ”resilience deficit,” characterized by high information mismatch (\(\text{JSD\ }\approx 0.024\)) and weak structural defense. Notably, the reservoir host johnsongrass (e.g., SH1350) maintained a high-return portfolio supported by strong structural defense (Data S1), illustrating a ”fortress” strategy that ensures persistence without pathogen elimination. In conclusion, sorghum defense is a multi-scale architecture where canopy physics, tissue barriers, and molecular allocation function as an integrated portfolio. Our findings suggest that breeding for ”efficient portfolios”—genotypes that align structural avoidance with information-guided molecular defense, offers a promising pathway to enhance crop resilience in a changing environment. More broadly, integrating structural traits, tissue‑specific susceptibility and information‑theoretic metrics may help unify tolerance and resistance concepts (Pagán & García-Arenal 2020) and provide a common language for comparing defense strategies across plant–pathogen systems and spatial scales (Garin et al. 2018; Runting et al. 2018). Authorship contribution statement Ezekiel Ahn: Writing – original draft, Supervision, Project administration, Methodology, Formal analysis, Data curation, Conceptualization. Insuck Baek: Writing – review & editing, Validation, Software, Resources. Louis K. Prom: Writing – review & editing, Resources. Seunghyun Lim: Writing – review & editing, Formal analysis. Sunchung Park: Writing – review & editing, Validation. Moon S. Kim: Writing – review & editing, Resources. Lyndel W. Meinhardt: Writing – review & editing, Resources. Clint Magill: Writing – review & editing, Methodology, Resources, Funding acquisition. Mention of any trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the U. S. Department of Agriculture. USDA is an equal opportunity provider and employer, and all agency services are available without discrimination. This work is supported by the U.S. Department of Agriculture, Agricultural Research Service, In-House Projects No. 8042-21220-258-000-D and 8042-21000-303-000-D. Conflicts of Interest The authors declare no conflicts of interest. Data availability All raw data underlying this study are provided in the accompanying archive “Raw data for ‘Multi-scale defense architecture in sorghum’ ” (file name: Raw_data.zip).This archive compiles the three primary input datasets derived from the authors’ previous experimental cohorts, harmonized for the current multi-scale analysis: 1. 8leaf_final.xlsx: Contains canopy leaf angle measurements and whole-plant disease severity scores from the 8-leaf stage experiments, originally described in Ahn et al. (2020; Sci. Rep.). These data were used to construct the canopy geometry manifold and calculate the structural defense index ( \(\lambda_{\text{arch}}\) ). 2. susceptibility score_Midrib.xlsx: Contains tissue-specific lesion scores comparing leaf blade versus midrib susceptibility, derived from the ”midrib fortress” assays detailed in Ahn et al. (2019; Physiol. Mol. Plant Pathol.). 3. qpcr_leaf_midrib_allocation.csv: Contains qPCR fold-change values for defense-related genes (e.g., PR-10, CHS8, Glucanase) in leaf and midrib tissues. These data, originating from the experimental context of Ahn et al. (2018; J. Plant Pathol. Microbiol.) and Ahn et al. (2019), were used to compute the defense allocation probability ( \(P_{\text{defense}}\) ) and information alignment (JSD). All derived tables, statistical outputs, and model parameters generated from these raw inputs are provided in Supplementary Data S1. The complete Python pipeline used to generate these outputs will be made publicly available in a GitHub repository and cited in the final version of the article once the manuscript is accepted. The script reproduces all steps described in the Methods, from raw data loading through model fitting and figure/table generation. Prior to publication, the code can be obtained from the corresponding author on reasonable request. Supporting Information The following supporting information can be found in the online version of this article: Methods S1. Detailed experimental procedures and statistical modeling. Figure S1. Principal Component Analysis of sorghum and johnsongrass canopy architecture. Figure S2. Correlation structure linking canopy geometry, physics indices, and disease severity. Figure S3. Structural defense equations linking canopy architecture to disease. Table S1. Summary of canopy angle traits per genotype Table S2. Information-theoretic alignment between attack and defense distributions. Supplementary Data S1. Consolidated Excel dataset containing all processed data tables corresponding to the figures and supplementary tables. References Ahn E., Odvody G., Prom L.K. & Magill C. (2020) Leaf angle distribution in Johnsongrass, leaf thickness in sorghum and Johnsongrass, and association with response to Colletotrichum sublineola. Scientific Reports 10 , 22320.Ahn E., Prom L.K. & Magill C. (2021) Diseases of Johnsongrass (Sorghum halepense): possible role as a reservoir of pathogens affecting other plants. Weed Science 69 , 393–403.Ahn E., Prom L.K., Odvody G. & Magill C. (2019) Defense responses against the sorghum anthracnose pathogen in leaf blade and midrib tissue of johnsongrass and sorghum. Physiological and Molecular Plant Pathology 106 , 81–86.Ahn E., Prom L.K., Odvody G.N. & Magill C.W. (2018) Responses of Johnsongrass against Sorghum Anthracnose isolates. Journal of Plant Pathology & Microbiology 09 , 1–6.Falster D.S. & Westoby M. (2003) Leaf size and angle vary widely across species: what consequences for light interception? New Phytologist 158 , 509–525.Garin G., Pradal C., Fournier C., Claessen D., Houlès V. & Robert C. (2018) Modelling interaction dynamics between two foliar pathogens in wheat: a multi-scale approach. Annals of botany 121 , 927–940.Pagán I. & García-Arenal F. (2020) Tolerance of plants to pathogens: a unifying view. Annual review of phytopathology 58 , 77–96.Runting R.K., Beyer H.L., Dujardin Y., Lovelock C.E., Bryan B.A. & Rhodes J.R. (2018) Reducing risk in reserve selection using Modern Portfolio Theory: Coastal planning under sea‐level rise. Journal of Applied Ecology 55 , 2193–2203.Xavier K., Mizubuti E., Queiroz M., Chopra S. & Vaillancourt L. (2018) Genotypic and pathogenic diversity of Colletotrichum sublineola isolates from sorghum (Sorghum bicolor) and johnsongrass (S. halepense) in the southeastern United States. Plant disease 102 , 2341–2351. Supplementary Material File (figure.zip) Download 1.11 MB Information & Authors Information Version history V1 Version 1 03 December 2025 Copyright This work is licensed under a Non Exclusive No Reuse License. Keywords canopy architecture defense portfolio genetic variation growth midrib defense sorghum anthracnose Authors Affiliations Eze Ahn 0000-0003-4447-4104 [email protected] USDA-ARS Beltsville Agricultural Research Center View all articles by this author Insuck Baek USDA-ARS Environmental Microbial & Food Safety Laboratory View all articles by this author Louis K. Prom USDA-ARS Southern Plains Agricultural Research Center View all articles by this author Seunghyun Lim USDA-ARS Beltsville Agricultural Research Center View all articles by this author Sunchung Park 0000-0002-7398-9476 USDA-ARS Beltsville Agricultural Research Center View all articles by this author Moon S. Kim USDA-ARS Environmental Microbial & Food Safety Laboratory View all articles by this author Lyndel W. Meinhardt USDA-ARS Beltsville Agricultural Research Center View all articles by this author Clint Magill Texas A&M University Department of Plant Pathology and Microbiology View all articles by this author Metrics & Citations Metrics Article Usage 293 views 150 downloads .FvxKWukQNSOunydq8rnd { width: 100px; } Citations Download citation Eze Ahn, Insuck Baek, Louis K. Prom, et al. Multi-scale defense architecture in sorghum: Canopy geometry, midrib fortresses, and information-aligned immune portfolios for ecological resilience. Authorea . 03 December 2025. DOI: https://doi.org/10.22541/au.176477982.26936740/v1 If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download. For more information or tips please see 'Downloading to a citation manager' in the Help menu . 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