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Poor shoot and leaf growth in Huanglongbing-affected sweet orange is associated with increased investment in defenses.

ABSTRACT: Citrus disease Huanglongbing (HLB) causes sparse (thinner) canopies due to reduced leaf and shoot biomass. Herein, we present results demonstrating the possible mechanisms behind compromised leaf growth of HLB-affected 'Valencia' sweet orange trees by comparing morphological, transcriptome, and phytohormone profiles at different leaf development phases (1. buds at the start of the experiment; 2. buds on day 5; . 3. leaf emergence; 4. leaf expansion; and 5. leaf maturation) to healthy trees. Over a period of 3 months (in greenhouse conditions), HLB-affected trees had ≈40% reduction in growth traits such as tree height, number of shoots per tree, shoot length, internode length, and leaf size compared to healthy trees. In addition, buds from HLB-affected trees lagged by ≈1 week in sprouting as well as leaf growth. Throughout the leaf development, high accumulation of defense hormones, salicylic acid (SA) and abscisic acid (ABA), and low levels of growth-promoting hormone (auxin) were found in HLB-affected trees compared to healthy trees. Concomitantly, HLB-affected trees had upregulated differentially expressed genes (DEGs) encoding SA, ABA, and ethylene-related proteins in comparison to healthy trees. The total number of cells per leaf was lower in HLB-affected trees compared to healthy trees, which suggests that reduced cell division may coincide with low levels of growth-promoting hormones leading to small leaf size. Both bud dieback and leaf drop were higher in HLB-affected trees than in healthy trees, with concomitant upregulated DEGs encoding senescence-related proteins in HLB-affected trees that possibly resulted in accelerated aging and cell death. Taken together, it can be concluded that HLB-affected trees had a higher tradeoff of resources on defense over growth, leading to sparse canopies and a high tree mortality rate with HLB progression.

SUBMITTER: Neupane A

PROVIDER: S-EPMC10766359 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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Poor shoot and leaf growth in Huanglongbing-affected sweet orange is associated with increased investment in defenses.

Neupane Answiya A Shahzad Faisal F Bernardini Chiara C Levy Amit A Vashisth Tripti T

Frontiers in plant science 20231219

Citrus disease Huanglongbing (HLB) causes sparse (thinner) canopies due to reduced leaf and shoot biomass. Herein, we present results demonstrating the possible mechanisms behind compromised leaf growth of HLB-affected 'Valencia' sweet orange trees by comparing morphological, transcriptome, and phytohormone profiles at different leaf development phases (1. buds at the start of the experiment; 2. buds on day 5; . 3. leaf emergence; 4. leaf expansion; and 5. leaf maturation) to healthy trees. Over ...[more]

PMID: 38179481

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Project description:To evaluate the transcriptome response of roots towards Hoagland solution of two-year-old healthy (C) and HLB-affected (T) sweet orange (Citrus sinensis L.) cultivar Midsweet grafted on Kuharskei Carrizo rootstock at three different time points; D1 (at the start of the experiment), D2 (After 3 days of Hoagland solution), D3 (After nine days of Hoagland solution), were performed using RNA sequencing analysis. A total of 9, 19, and 2324 DEGs were expressed in HLB-affected and healthy trees feeder roots on D1, D2, and D3, respectively. Due to a small number of DEGs in HLB-affected and healthy trees roots on D1 and D2, enrichment analysis could not be performed. At D3, Gene Ontology (GO) enrichment analysis was performed using upregulated and downregulated DEGs in HLB-affected roots compared to healthy roots. For the upregulated DEGs in HLB-affected roots, the most enriched biological GO categories were related to transport, cellular amino acid metabolic process, oxoacid metabolic process, organic acid metabolic processes, phenylpropanoid biosynthesis process, response to carbohydrate stimulus, ethylene and the jasmonic acid-mediated signaling pathway, and regulation of plant hormone. The biological GO categories based on the number of DEGs associated with downregulated DEGs were the developmental process, phosphate metabolic process, protein modification process, defense response, growth, cell cycle, cell death, and ABA-mediated signaling pathway. The results of this study strongly suggest; although, the reduced biomass limits the nutrient uptake capacity in the plants as a whole, so in order to compensate for reduced root to shoot ratio the existing root undergo anatomical and transcriptomic changes to improve nutrient uptake efficiency to meet the nutrient demand of shoot systems. It is likely that higher inputs of energy in nutrient uptake possibly results in reducing the root longevity of HLB-affected trees. Good nutrition management practices are critical for the survival of HLB-affected trees as the availability and uptake of nutrients allow HLB-affected trees in response to abiotic and biotic stress.

Project description:The Brazilian citrus orchards are comprised by few genotypes, which increases the risk of pest and disease outbreaks. The diversification of sweet oranges (Citrus × sinensis) in orchards also generates off-season revenue and extend the fruit processing period. This study aimed to evaluate several horticultural traits of 19 late-season sweet orange selections under citrus canker and huanglongbing (HLB) endemic condition in northwestern Paraná state, Brazil, in a long-term field experiment. Tree size, yield, fruit quality for fresh fruit and industrial markets, estimates of tree density and yield, and citrus canker and huanglongbing (HLB) incidences were assessed. The experimental design was a randomized block with three replicates and five trees per unit. The orchard was drip-irrigated and arranged at tree spacing of 6.5 m × 4.5 m. All scions were graft-compatible with Rangpur lime (C. × limonia). Valencia selections had the tallest trees and largest canopies, particularly Olinda, Frost and #121 with heights and volumes greater than 4.20 m and 43 m3, respectively. Natal África do Sul and Whit's Late Valencia trees were the most productive with cumulative yields above 640 kg per tree. Most of the selections produced fruits of excellent physicochemical quality attending the fresh fruit and industrial market requirements. All selections showed similar horticultural characteristics for the fresh market, while Natal África do Sul and Charmute de Brotas were more suitable for juice processing. Frost Valencia and Valencia Late Fla. had the highest incidence of citrus canker on fruits (>20%), whereas IPR Folha Murcha, Charmute de Brotas and some Valencia selections (Chafeei Late, Campbell 479, Campbell 294, Olinda, Mutação and Whit's Late) exihibed low incidence (3.0-17.7%). At 9 years, Valencia Mutação trees had high HLB incidence (93%). In contrast, Natal IAC and Folha Murcha IAC showed the lowest HLB incidence (13%). Our results revealed that Natal IAC, Folha Murcha IAC, IPR Folha Murcha, Natal Murcha, Campbell 479 Valencia and Valencia Late Fla. had the best horticultural performance in addition to low HLB incidence. Together, these late-season sweet oranges are the most advantageous selections for citrus orchard diversification under citrus canker and HLB endemic conditions in humid subtropical regions.

Project description:BACKGROUND:Citrus blight is a very important progressive decline disease of commercial citrus. The etiology is unknown, although the disease can be transmitted by root grafts, suggesting a viral etiology. Diagnosis is made by demonstrating physical blockage of xylem cells that prevents the movement of water. This test was used to identify symptomatic trees from four commercial groves in Florida. Total RNA extracts of phloem-enriched scaffold root tissues were prepared from seven trees that failed to take up water and from one healthy tree. These RNA extracts were used for transcriptomic analyses using paired end RNA-Seq from an Illumina 2500 system. The expression of transcripts annotated as polyprotein of citrus endogenous pararetrovirus were estimated by both RT-qPCR and RNA-Seq. RESULTS:Transcripts from seven RNA-Seq libraries from trees affected by citrus blight were compared to a control tree. 129-148 million RNA fragments (two paired-end reads/fragment) were generated per library and were mapped to the sweet orange reference genome. In response to citrus blight stress, genes encoding aquaporins, proteins with water channel activity and several cellulose synthase genes were down-regulated, whereas genes involved in lignin and glucosinolate biosynthesis were up-regulated. Transcripts encoding proteins in pathways of carbohydrate metabolism, nucleotide synthesis, signaling, hormone metabolism, secondary metabolism, transport, and biotic stress pathways were overwhelmingly down regulated in all libraries. CONCLUSION:Reduced water intake and xylem plugging were observed in the trees tested and the changes in their transcriptome were analyzed. Plants adapted to reduced water flow by regulating primary and secondary metabolism, nuclear transport and hormone associated pathways. The patterns of energy generation, transcription, translation and protein degradation were consistent with irreversible decline. The down regulation of cellulose synthase transcripts and up regulation of transcripts related to lignin production likely lead to an imbalance in the pathways leading to wood formation, and may lead to the blockage of the xylem vessels seen as the cardinal symptom of citrus blight. Transcripts of a pararetrovirus were elevated in the transcriptome of roots used in this study.

Dataset Information

Poor shoot and leaf growth in Huanglongbing-affected sweet orange is associated with increased investment in defenses.

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Poor shoot and leaf growth in Huanglongbing-affected sweet orange is associated with increased investment in defenses.

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