Introduction
Phytoplasmas are very small bacteria lacking a cell wall but causing
severe plant diseases to a number of important agricultural crops. They
cause a bundle of symptoms in their respective host plants.
‘Candidatus Phytoplasma’ species of the group 16SrX include three
economically important disorders of temperate fruit trees: The diseases
apple proliferation (AP), pear decline (PD) and European stone fruit
yellows (ESFY), which are of high economic significance, causing crop
losses just in Europe of around half a billion Euro a year (Eurostat
2009; Strauss, 2009). Like the host plants of the 16SrX phytoplasmas
that all belong to the Rosaceae, the causing agents of these diseases
’Candidatus Phytoplasma mali’, ’Candidatus Phytoplasma
pyri’ and ’Candidatus Phytoplasma prunorum’, are phylogenetically
closely related and believed to be indigenous to Europe (Jarausch et
al. , 2019a; Seemüller & Schneider, 2004). These phytoplasmas
have small linear chromosomes and lack many genes encoding important
metabolic functions, such as amino and fatty acid synthesis (Kube et
al., 2008; Oshima et al. , 2013). Therefore, they need to consume
essential metabolites from their plant hosts.
Phytoplasmas are restricted to the phloem sieve elements in their host
plants (Seemüller, 2002; Zimmermann et al., 2015). The phloem
serves as main route for the long and short‐distance transport of mainly
organic compounds (Hafke et al., 2005; van Bel, 1996). Sieve elements
(SEs), companion cells (CCs) and phloem parenchyma cells (PPCs) are the
three phloem cell types involved also in transport of defence- and
stress related signalling molecules, such as RNA, proteins, and
phytohormones (e.g. Dempsey & Klessig, 2012; Furch et al., 2014; Jung
et al., 2009; Park et al., 2007). The sieve element sap is
an energy-rich environment, sustaining phytoplasmas with nutrients and
enabling them to distribute all over the plant. Therefore, an impairment
of the phloem cells and a change in the phloem sap composition is most
likely.
The distribution of secondary compounds plays a crucial role in plant
communication and the induction of defence mechanisms against invading
pathogens and attacking herbivores. It was previously shown that
phytoplasmas produce and secrete effector proteins into phloem cells
that induce physiological changes in infected host plants (Sugio et
al. , 2011a). A number of non-specific symptoms, such as
chlorosis, leaf yellowing, premature reddening, swollen leaf-veins, leaf
curl and reduced vigor might be attributed to the impairment of the
vascular system and the photosynthesis apparatus (Bertamini et al.,
2002; Bertamini et al. , 2004; Maust et al., 2003). Additionally,
abnormal growth, stunting, growth of witches’ brooms, reduced root size
and dwarf fruits occur in phytoplasma infected plants indicating a
disturbed hormone balance (Dermastia, 2019). Phytohormones are induced
in reaction to abiotic and biotic stresses and lead to the induction of
defense responses (Walling, 2000). The influence of phytoplasma
infections on salicylic acid, jasmonates, auxins, abscisic acid,
ethylene and cytokinine biosynthesis and pathways was recently reviewed
by Dermastia (2019), illustrating the diverse and complex interactions
between the specialized pathogens and their host plants.
In the case of phytoplasmas, we have to take into consideration the
impact on vector insects that are crucial for the distribution of
phytoplasmas. So far, all phytoplasmas of the group 16SrX causing
important fruit crop diseases are vectored by jumping plant lice
(Hemiptera: Psylloidea) or succinctly psyllids (Jarausch et al., 2019b).
Psyllids are phloem feeders and both nymphs and adults feed on plant
phloem and occasionally on xylem sap, too (Gallinger & Gross, 2018,
2020; Weintraub & Beanland, 2006). Therefore, morphological changes of
the plant vascular system may affect psyllid feeding behaviour and
suitability of host plants. Additionally, phloem/xylem components may
influence host choice and oviposition behaviour of psyllids (Gallinger
& Gross, 2018, 2020; Mayer et al., 2011). In addition, to detect
appropriate host plants for feeding and reproduction, volatile signals
are used by many vectoring psyllids species during migration (Gallinger
et al., 2019, 2020; Gross & Mekonen, 2005; Mayer et al. ,
2008a,b, 2009; Soroker et al. , 2005; Weintraub & Gross, 2013).
As often plant volatile emission is regulated by phytohormones their
changes in concentrations play an important role on the interplay of
vector insects, plants and phytoplasmas (Gross, 2016).
Intra- and interspecific differences in the response of fruit trees to
phytoplasma diseases have been observed over the last decades under both
experimental and natural infection conditions (Fiore et al., 2019;
Marcone & Rao, 2019). However, only few studies provide firm data on
host response, host–pathogen interaction and on anatomical,
physiological and molecular basis of resistance (Seemüller & Harries,
2010), which is still poorly understood (Marcone & Rao, 2019).
In the present study, we explored how infections with specific fruit
tree phytoplasmas (‘Ca .P. mali’, ‘Ca . P. pyri’ and
‘Ca . P. prunorum’) belonging to the 16SrX group (Seemüller &
Schneider, 2004), changed important morphological and physiological
parameters of their respective host plants belonging to the same plant
family, the Rosaceae (Potter et al., 2007). We measured typical
parameters such as leaf morphology, plant vascular morphology and
callose deposition, determined physical phloem parameters (mass flow
velocity and volumetric flow rate, relative density and dynamic
viscosity), and analysed the content of several phytohormones in leaf
tissues of healthy and phytoplasma-infected plants. The importance of
measured parameters for symptom manifestation as well as the impact on
vector insects and phytoplasma spread is discussed.