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.