2018 ASHS Annual Conference

Reniform nematode (Rotylenchus reniformis, RN) is a sedentary plant-parasitic nematode that infects over 300 species from numerous plant families in tropical, subtropical, and warm-temperate regions. Among its hosts are multiple economically-important crops, including pineapple, soybean, and cotton. Belowground parasitism by RN involves anatomical and metabolic changes in root pericycle cells, the same cells from which lateral roots emerge. We investigated the effect of RN parasitism on root growth, architecture and histology in upland cotton (Gossypium hirsutum) and documented the expression of multiple genes related to lateral root development and auxin dynamics in parasitized roots. Nematode-induced changes in root growth were measured in three plant culture systems: split-root pots, foam cups, and germination pouches. Gene expression of infected and uninfected roots was measured using Illumina-based RNA sequencing, followed by Trinity de novo transcriptome assembly and transcript quantification with rsem and DESeq2.

At 3 days after inoculation (DAI), RNs had penetrated cotton roots intracellularly; some nematodes had arrived at the endodermis. At this stage, the pericycle cells surrounding the nematode head were not visibly modified. By 9 DAI, expanding feeding sites (syncytia) were clearly visible as regions of hypertrophied, interconnected pericycle cells filled with dense cytoplasm, enlarged nuclei and nucleoli, and an increased number and size of organelles. Across multiple plant culture systems, nematode parasitism increased total root length, weight, branching, and fractal dimension. Simultaneously, the expression of multiple genes associated with lateral root development and with auxin metabolism, transport, and response were altered in parasitized roots. Of particular note was the up-regulation at 3 DAI of Lateral Root Primordium 1, an auxin-regulated transcription factor whose Arabidopsis homolog is expressed in developing lateral root primordia. Also strongly induced in early parasitism were genes encoding the auxin biosynthetic enzyme YUCCA10 and an auxin polar transporter from the ABC family. Later stages of parasitism were characterized by the differential expression of additional auxin transporters, auxin response factors, and lateral root-associated genes. The increased production of lateral roots in parasitized plants may result from nematode manipulation of the plant’s own hormonal pathways. Alternately it may reflect increased allocation of carbon to root growth in response to the strong sink produced by nematode feeding. A larger root system may ultimately benefit the parasite by increasing the root surface area available for feeding by its offspring.