- HUANGLONGBING: DEVASTATING DISEASE OF CITRUS 333
contact between plant and microbe. Honeycrisp apples are prone to
zonal chlorosis in leaves in the absence of any pathological agent, this
disorder has been shown to be related to the accumulation of excess
starch in chloroplasts (Chen and Cheng 2004; Snyder-Leiby and Wang
2008). In Arabidopsis and tomatoes, feeding by the green peach aphid
stimulates the accumulation of starch in the absence of phloem plug-
ging (Singh and Shah 2012). There is a strong correlation between
CLas titer in leaves and starch content in leaves and roots. Increases
in leaf starch and decreases in root starch could be detected in small
greenhouse-grown Valencia sweet orange when CLas titers were less
than 100 cells per mg plant tissue and this effect was exacerbated as
titer increased (McCollum and Hall, unpublished). Visible HLB symp-
toms do not appear until CLas titer exceed about 1000 copies per mg
tissue, coincident with the most rapid increase in starch accumulation
(McCollum et al. 2014). Excessive accumulation of starch can lead to
chloroplast disruption and chlorosis in citrus (Schaffer et al. 1986) and
in apples (Chen and Cheng 2004; Snyder-Leiby and Wang 2008). In
HLB-symptomatic tissue, cholorplast’s outer membranes were intact,
but inner granna structure was disrupted (Achor et al. 2010) suggesting
that this may be the basis for the chlorosis that occurs in CLas-infected
leaves.
Starch accumulation can be the consequence of increased synthesis,
decreased degradation, or a combination of the two. Fan et al. (2010)
found that the concentration of maltose was reduced by ca. 50% in
CLas-infected leaves whether they were asymptomatic or symptomatic.
Maltose is the predominant form of carbon exported from chloroplasts
at night, and maltose increases in leaves when starch breakdown is
induced (Lu and Sharkey 2006). The decrease in maltose seen in CLas-
infected leaves (Fan et al. 2010) suggests that the breakdown of starch
is inhibited, and may contribute to starch accumulation.
Rawat et al. (2015) conducted a meta-analysis using data from 22
published transcriptomic studies on citrus–CLas interactions and found
that transcripts for carbohydrate metabolism represented one of the core
pathways affected in CLas-infected tissues. In addition, transcriptomic
analyses of CLas-infected tissue indicate an increase in abundance of
transcripts for adenosine diphosphate glucose phosphorylase (ADGP)
(Albrecht and Bowman 2008), the rate limiting enzyme in starch biosyn-
thesis, suggesting that increase in activity of this enzyme may be related
to the abnormal accumulation of starch. Although ADPG phosphorylase
transcripts are more abundant in CLas-infected than in non-infected
tissues, ADPGase activity is not well correlated with transcript abun-
dance, but rather with posttranslational modification (Hadrich et al. ̈