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Citrus Greening Transcriptome Study Hints at Mechanism, Possible Treatments

NEW YORK (GenomeWeb News) – Infection with the citrus disease huanglongbing wreaks havoc on both plants' ability to regulate their sugar metabolism and their hormonal networks, according to a study appearing in PLOS One yesterday.

Through transcriptome and functional analysis of a variety of plant tissues with different diseases statuses, the researchers led by Abhaya Dandekar, a professor at the University of California, Davis, found that the bacteria behind the disease affects sugar and starch metabolism in young and mature fruits and leaves while also inducing changes in jasmonic acid synthesis that may, in turn, affect plants' immune response.

The disease is caused by three species of closely related bacteria — Candidatus Liberibacter asiaticus, Ca. L. africanus, and Ca. L. americanus — that are transmitted from plant to plant through a citrus psyllid that flies between plants, feeding on them while also picking up and distributing the bacteria.

As the name implies, citrus greening leads to discolored fruit, which also is misshapen, hardened, and bitter. The disease also affects the leaves, causing them to accumulate starch, turn yellow, and become blotchy. In addition, the phloem is damaged, and seeds of the plant are rendered unviable. Infected plants typically die within a few years.

"Because the disease has a long latent phase during which there are no symptoms of infection and the bacteria are resistant to being grown in the laboratory, the only option for halting transmission of citrus greening has been to apply chemical pesticides to control the insect that spreads the bacteria," Dandekar said in a statement.

This new study, though, suggests that the disease may be able to be managed through the use of hormones and other small molecules.

The US citrus industry in 2012 was valued at $3.4 billion, and huanglongbing is a threat to that sector, according to UC-Davis. Currently, the disease is widespread in Florida, and while only one tree in California is known to have been infected with citrus greening, the psyllid that transmits the bacteria has been found up and down Southern California and into the Central Valley.

Previous genomic studies of the CaLa bacteria behind the disease found no toxins, no cell-wall degrading enzymes, nor a secretion system that could hint at how they had their effect, Dandekar and his colleagues noted, adding that they thus suspected that the disease stems from metabolic imbalances and disruptions to nutrient transport in infected plants.

To study how infection with CaLa bacteria affects citrus plants, Dandekar and his colleagues obtained tissue samples from immature and mature fruit and from young and mature leaves from apparently healthy, asymptomatic, symptomatic, and disease-free plants. On all of these samples, they performed RNA-seq, generating a total of 889 million paired-end reads that they aligned to the Citrus sinensis, or orange, genome.

Overall, a principal component analysis grouped the samples into three expression profiles: leaves, immature fruit, and mature fruit.

Infection with huanglongbing, though, altered both the fruit and leaf transcriptomes.

For example, in fruit, the bacteria appeared to regulate sucrose degradation and starch biosynthesis genes, while a number of metabolism-related genes were overexpressed.

Meanwhile in the leaves, there was a downregulation of photosynthesis, Calvin cycles, and photorespiration genes, while sucrose and starch metabolism genes were upregulated, confirming a previous finding that the diseases lead to an accumulation of starch in the leaves. In mature leaves, the researchers noted, those mechanisms were severely affected.

"[T]he pathogen differentially affects sugar and starch metabolism in young and mature leaves and fruits. The upregulation of [the glucose-phosphate transporter] GPT in young leaves was key to inducing starch accumulation, with a consequent decrease in photosynthesis," the researchers said. "The upregulation of sucrose metabolism added to the source-sink metabolic dysfunction that, in our opinion, is the most probable cause of the disease."

Additionally, huanglongbing infection affects the plants' hormone crosstalk and response to that infection, the researchers reported. Although the methylsalicylic acid transferase gene was upregulated in young infected leaves, salicylic acid signaling and salicylic acid-mediated defense were not highly activated in infected plants. Other activated genes in the related jasmonic signaling pathway were also upregulated and that, the researchers said, could confuse the salicylic response.

These effects of the huanglongbing bacteria on the plants' transcriptomes, though, hint at possible lines of treatment, beyond the currently used pesticides that target the insect vector. "Using hormones and other small molecules holds promise to reverse the metabolic dysfunction and improve the innate immune response to this devastating disease of Citrus," Dandekar and his colleagues said.