<i>Hamiltonella</i> symbionts benefit whitefly fertilization by regulating the maternal protein Tudor-mediated piRNA pathway.

Abstract

Although it is widely recognized that nutritional symbionts can manipulate host reproduction, the underlying molecular and cellular mechanisms are largely unclear. The facultative symbiont <i>Hamiltonella</i> in bacteriocyte induces female-biased sex ratio of whiteflies. Here, we demonstrate that a maternal gene <i>tudor</i> (<i>tud</i>) and its encoded protein have lower expression levels in ovaries of <i>Hamiltonella-</i>cured whiteflies. Tud family proteins can interlink the various stages of biosynthesis of PIWI-interacting RNA (piRNA), a class of small noncoding RNAs. We find that <i>Hamiltonella</i> affects the abundance of a piRNA through the maternal gene <i>tud</i>, thereby regulating the expression of the <i>vacuolar</i> (<i>H+</i>)<i>-ATPase H subunit</i> (<i>VATPH</i>), which is the switch of activity of the vacuolar (H+)-ATPase that plays a crucial role in maintaining the homeostasis of intracellular energy and supporting mitochondrial respiration. This regulation adjusts the ATP level in ovaries of whiteflies. The ATP level shapes the F-actin pattern in ovaries and eggs of whiteflies, ultimately manipulating whitefly fertilization. Silencing <i>tud</i> inhibited whitefly fertilization by impairing ATP levels and F-actin patterns in ovaries and eggs. This study reveals that symbiont and maternal protein associations can regulate host fertilization by piRNA biosynthesis.