Ann Appl Biol.2013 162(2):191-199.

Role of gibberellic acid in tomato defense against potato purple top phytoplasma infection

Yang Dinga,b, Wei Weib, Wei Wub, Robert E. Davisb, Yi Jiangb, Ing-Ming Leeb, Rosemarie W. Hammondb, Lin Shena, Ji-Ping Shenga, and Yan Zhaob,*

aCollege of Food Science and Nutritional Engineering, China Agricultural University, Beijing 100083, China. bMolecular Plant Pathology Laboratory, USDA-Agricultural Research Service, Beltsville, MD 20705, USA.

*Correspondence: Yan Zhao; Tel: +1 301-504-6202; Email: yan.zhao@ars.usda.gov

 

Abstract:

Infection of tomato by potato purple top (PPT) phytoplasma causes disruption of gibberellin (GA) homeostasis in the plant host. Such pathologically-induced GA deficiency can be partially reversed by exogenous application of GA.  The present study was designed to explore the role of GA in tomato defense response against phytoplasmal disease, and to determine whether pretreatment with GA would protect healthy tomato seedlings from subsequent phytoplasmal infection and disease development. Our results revealed that, following exogenous GA application and subsequent PPT phytoplasma graft inoculation, there was an apparently coordinated down-regulation of the gene encoding a key GA signaling component and growth repressor known as DELLA protein  (GAI) and up-regulation of genes involved in salicylic acid (SA) synthesis (ICS1), signaling (NIM1), and downstream defense responses (PRP-1).  Our results also indicated that differential regulation of the above genes was correlated with an increase in activities of defense-related enzymes β-1,3-glucanase (GLU) and chitinase (CHI). The data presented in this communication provide evidence to suggest that GA may act via DELLA and SA signaling pathways to modulate host defense in response to PPT phytoplasma infection.  Although the GA pretreatment-induced defense was not sufficient to prevent a systemic infection, it reduced phytoplasma titer and significantly attenuated disease symptoms. While the actual molecular mechanism underlying the GA-induced plant defense remains elusive, findings from the current study open new opportunities for in-depth studies of the functional role of the GA signaling network during defense response against phytoplasmal infection.

 

Supplement:

(Phytoplasma-host interactions: tomato gibberellin homeostasis and its role in defense against potato purple top phytoplasma infection)

Phytoplasmas are cell wall-less bacteria that parasitize plant phloem sieve cells and cause numerous diseases in diverse plant species.  Plants infected by phytoplasmas often exhibit symptoms such as general stunting, excessive shoot proliferation, witches’-broom growth, rapid senescence, and abnormal floral development. Such growth and developmental abnormalities are suggestive of a profound perturbation in plant hormone balance.  In a previous study, we found that phytoplasma infection caused a significant reduction in endogenous levels of gibberellic acid (GA3), one of the key plant hormones.  The decrease in GA3 content in diseased plants was correlated with down regulation of genes responsible for biosynthesis of bioactive GAs.  Our results further suggested that there was a diminished sensitivity of the GA biosynthesis negative feedback regulation under the conditions of phytoplasma infection.  We also found that exogenous application of GA3 was able to partially reverse the pathologically-induced GA deficiency, therefore attenuating certain phytoplasmal disease symptoms.  These findings led us to hypothesize that GA plays a role in plant defense against phytoplasma infection.

In the present study, we tested our hypothesis and attempted to determine whether pretreatment with GA would protect healthy plants from subsequent phytoplasmal infection and/or impede disease development.  We used potato purple top (PPT) phytoplasma and its host tomato as a pathogen-host pair in our experiment.  Our results revealed that, following exogenous GA application and a subsequent graft-inoculation of the treated plants with PPT phytoplasma, there was an apparently coordinated transcriptional reprogramming of a suite of host genes:  down-regulation of the gene encoding a key GA signaling component and growth repressor known as DELLA protein and up-regulation of genes involved in salicylic acid (SA) synthesis, signaling, and downstream defense responses.  For instance, at three days post inoculation (3-dpi), the expression levels of the host gene encoding the SA biosynthesis enzyme isochorismate synthase 1 (ICS1) increased in phytoplasma-infected plants that were pretreated with GA.  Likewise, the transcript levels of the gene encoding an important SA signaling component named noninducible immunity protein (NIM1) were elevated in GA-pretreated plants at 3dpi.  Furthermore, the expression of the PRP-1 gene, a molecular marker of SA-induced systemic acquired resistance, was also up-regulated in GA-pretreated, infected plants starting at 3-dpi.  Our results also indicated that differential regulation of the above genes was correlated with an increase in activities of defense-related enzymes β-1,3-glucanase and chitinase.  Although the GA pretreatment-induced defense was not sufficient to prevent a systemic infection by the phytoplasma, it effectively reduced phytoplasma titer and significantly attenuated disease symptoms.

Plant hormones play crucial roles in mediating multiple developmental processes and cellular responses to biotic and abiotic stresses. Several naturally occurring plant hormones, such as gibberellins, auxins, abscisic acid, cytokinins, salicylic acid, jasmonic acid (JA), ethylene (ET), and brassinosteroids, have been implicated in pathogen-host interactions.  Much progress has been made in elucidation of SA, JA, and ET signaling pathways that are triggered by microbial attack.  Recent studies revealed that exogenous application of SA or its functional analogue, benzothiadiazole (BTH), could activate plant defense response against various phytoplasmal diseases.  The benefit of SA or BTH treatment on phytoplasma-infected plants included delaying symptom development, reducing symptom severity and, in some cases, achieving a higher rate of symptom remission.  In addition, SA application was able to prime the defense system of healthy tomato seedlings against subsequent attack by the PPT phytoplasma, significantly reducing the rate of infection and impeding disease advancement in those plants that became infected.  Results from our work provide evidence to suggest that GA can also modulate plant defense in response to phytoplasma infection via DELLA and SA signaling pathways.

Despite recent advances in phytoplasma research, the underlying mechanisms of phytoplasmal pathogenesis and plant defense against phytoplasmal diseases remain poorly understood.  We hope the findings from our work will open new opportunities for in-depth studies on the functional role of the GA signaling network during phytoplasma-host interaction, and speed development of practical approaches toward phytoplasmal disease mitigation.

Yan Zhao-1

Figure legend: A proposed model of phytoplasma infection-induced disruption of gibberellin homeostasis and possible role of bioactive GA in plant defense against phytoplasmal disease.

 

References:

  1. Ding Y., Wu W., Wei W., Davis R.E., Lee I.-M., Hammond R.W., Sheng J.P., Shen L., Jiang Y., and Zhao Y. (2013) Potato purple top phytoplasma-induced disruption of gibberellin homeostasis in tomato plants. Annals of Applied Biology, 162:131-139.
  2. Wu W., Ding Y., Wei W., Davis R.E., Lee I.-M. Hammond R.W., Zhao Y. (2012) Salicylic acid-mediated elicitation of tomato defense against infection by potato purple top phytoplasma. Annals of Applied Biology, 161:36-45.
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