Integrating below- and above-ground signaling in Nicotiana attenuata : root oxylipins systemically regulate leaf responses to attack and increase plant resistance

In this thesis, I investigate the role of the roots in processes which have so far mostly described within leaves. I manipulate gene function in the roots, and ask whether root gene function affects plant responses to above-ground herbivore attack and above-ground herbivore preference. I establish an efficient micrografting protocol for N. attenuata, which consists of fusing two plant genotypes, one for the shoots and the other for the roots. By comparing non-grafted and grafted wild-type (WT) plants, I demonstrated that the damage micrografting inflicts does not comprise the growth and development of grafted plants. In addition, I show that in grafts combining silenced transgenic shoots to WT roots, the gene expression in WT roots is silenced by systemic post-transcriptional gene silencing (PTGS) in a shoot-to-root fashion. Further, with grafted plants impaired in root jasmonic acid (JA) synthesis or perception, I also demonstrate that nicotine accumulated in systemic leaves in response to leaf wounding is almost fully dependent on JA perception by coronatine insensitive1 (COI1) in the roots. De novo JA synthesis, which occurs in roots by the action of allene oxidase cyclase (AOC), is necessary but not sufficient to launch maximum nicotine levels upon leaf wounding. Next, I show that COI1 and AOC activity in roots regulates nicotine production in response to leaf wounding at the transcriptional level of nicotine biosynthesis in roots. In addition, COI1 and AOC activity in roots regulates the systemic transport of nicotine in the leaves. Most strikingly, I show a novel shoot-to-root loop that regulates local JA response upon leaf wounding, since JA is over-accumulated in damaged leaves of plants deprived of root JA. Moreover, under glasshouse and field conditions, I observe that root JA signaling influences herbivore performance and preference, and that root JA signaling is employed in an herbivore-specific way.


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