Effector biology during biotrophic invasion of plant cells

Chaudhari, Prateek; Ahmed, Bulbul; Joly, David L; Germain, Hugo

It should not be difficult to conceptualize massive host cellular reprogramming occurring in response to the development of haustoria. Haustoria are found to be surrounded by endoplasmic reticulum, actin cytoskeleton and cytoplasm, along with the accumulation of Golgi bodies and mitochondria. 54 It has also been observed that a significant amount of tonoplast is present around these complexes. 54 To host such critical appendages, cells have to expand their plasma membrane tremendously. Haustoria are separated from the host cytoplasm by an extrahaustorial matrix (EHM). The EHM has been speculated to be mostly of host origin, sealed from haustoria by a hautorial neck band. 55, 56 However, it differs from the plasma membrane in both cytological and biochemical properties. 55, 57 The EHM also appears to vary in composition over time. 58, 59 Recently, Lu et al. 60 reported that some plasma membrane resident proteins relocalize to the extra-haustorial membrane during infection. For example, the aquaporin PIP1;4 and the calcium ATPase ACA8 remained at the plasma membrane during infection with either H. arabidopsidis or Phytophtora infestans while the syntaxin PEN1 (penetration deficient 1), the synaptotagmin SYT1 and the remorin StREM1.3 were present in the extra-haustorial membrane around P. infestans haustoria. Interestingly, this relocalization appears to be pathogen-dependent since PRR FLS2 localized in the EHM of P. infestans but remained at the plasma membrane and was excluded from the EHM in H. arabidopsidis. However, the most remarkable feature of this cellular rearrangement is the position of the nucleus. Studies have shown that the Arabidopsis nucleus stays close to H. arabidopsidis haustoria, 30 and this is presumably driven by the actin cytoskeleton. 61, 62 It is possible that proximity of haustoria to the nucleus enables pathogens to deliver their effectors more quickly to the nucleus for cell reprogramming. Proximity of the nucleus to the intruder would thus be driven by the pathogen per se, but one cannot exclude that host plants could steer this process autonomously to respond quickly to pathogen attack.