AUTHOR=Abril-Urias Patricia , Ruiz-Ferrer Virginia , Cabrera Javier , Olmo Rocio , Silva Ana Cláudia , Díaz-Manzano Fernando Evaristo , Domínguez-Figueroa Jose , Martínez-Gómez Ángela , Gómez-Rojas Almudena , Moreno-Risueno Miguel Ángel , Fenoll Carmen , Escobar Carolina 

TITLE=Divergent regulation of auxin responsive genes in root-knot and cyst nematodes feeding sites formed in Arabidopsis

JOURNAL=Frontiers in Plant Science

VOLUME=14

YEAR=2023

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2023.1024815

DOI=10.3389/fpls.2023.1024815

ISSN=1664-462X

ABSTRACT=<p>Cysts (CNs) and root-knot nematodes (RKNs) induce specialized feeding cells, syncytia, and giant cells (GCs), respectively, within plant roots. The plant tissues around the GCs usually by respond forming a root swelling called a gall that contains the GCs. The ontogenesis of feeding cells is different. GC formation is a process of new organogenesis from vascular cells, which are still not well characterized, that differentiate into GCs. In contrast, syncytia formation involves the fusion of adjacent cells that have already differentiated. Nonetheless, both feeding sites show an auxin maximum pertinent to feeding site formation. However, data on the molecular divergences and similarities between the formation of both feeding sites regarding auxin-responsive genes are still scarce. We studied genes from the auxin transduction pathways that are crucial during gall and lateral root (LR) development in the CN interaction by using promoter-reporter (GUS/LUC)transgenic lines, as well as loss of function lines of Arabidopsis. The promoters <italic>pGATA23</italic> and several deletions of <italic>pmiR390a</italic> were active in syncytia, as were in galls, but <italic>pAHP6</italic> or putative up-stream regulators as <italic>ARF5/7/19</italic> were not active in syncytia. Additionally, none of these genes seemed to play a key role during cyst nematode establishment in Arabidopsis, as the infection rates in loss of function lines did not show significant differences compared to control Col-0 plants. Furthermore, the presence of only canonical AuxRe elements in their proximal promoter regions is highly correlated with their activation in galls/GCs (<italic>AHP6</italic>, <italic>LBD16</italic>), but those promoters active in syncytia (<italic>miR390</italic>, <italic>GATA23</italic>) carry AuxRe overlapping core <italic>cis</italic>-elements for other transcription factor families (i.e., bHLH, bZIP). Strikingly, <italic>in silico</italic> transcriptomic analysis showed very few genes upregulated by auxins common to those induced in GCs and syncytia, despite the high number of upregulated IAA responsive genes in syncytia and galls. The complex regulation of auxin transduction pathways, where different members of the auxin response factor (ARF) family may interact with other factors, and the differences in auxin sensitivity, as indicated by the lower induction of the <italic>DR5</italic> sensor in syncytia than galls, among other factors, may explain the divergent regulation of auxin responsive genes in the two types of nematode feeding sites.</p>