The Arabidopsis transcription factor TCP9 modulates root architectural plasticity, reactive oxygen species‐mediated processes, and tolerance to cyst nematode infections

Abstract

SUMMARY Infections by root‐feeding nematodes have profound effects on root system architecture and consequently shoot growth of host plants. Plants harbor intraspecific variation in their growth responses to belowground biotic stresses by nematodes, but the underlying mechanisms are not well understood. Here, we show that the transcription factor TEOSINTE BRANCHED/CYCLOIDEA/PROLIFERATING CELL FACTOR‐9 (TCP9) modulates root system architectural plasticity in Arabidopsis thaliana in response to infections by the endoparasitic cyst nematode Heterodera schachtii. Young seedlings of tcp9 knock‐out mutants display a significantly weaker primary root growth inhibition response to cyst nematodes than wild‐type Arabidopsis. In older plants, tcp9 reduces the impact of nematode infections on the emergence and growth of secondary roots. Importantly, the altered growth responses by tcp9 are most likely not caused by less biotic stress on the root system, because TCP9 does not affect the number of infections, nematode development, and size of the nematode‐induced feeding structures. RNA‐sequencing of nematode‐infected roots of the tcp9 mutants revealed differential regulation of enzymes involved in reactive oxygen species (ROS) homeostasis and responses to oxidative stress. We also found that root and shoot growth of tcp9 mutants is less sensitive to exogenous hydrogen peroxide and that ROS accumulation in nematode infection sites in these mutants is reduced. Altogether, these observations demonstrate that TCP9 modulates the root system architectural plasticity to nematode infections via ROS‐mediated processes. Our study further points at a novel regulatory mechanism contributing to the tolerance of plants to root‐feeding nematodes by mitigating the impact of belowground biotic stresses.

Physiological Roles and Mechanisms of Action of Class I TCP Transcription Factors

“…In soybean and eggplant, GmTCP19-Like (GmTCP19L) and SmTCP7a modulate resistance to Phytophthora sojae [ 22 ] and R. solanacearum [ 114 ], respectively, but the molecular mechanisms involved are still unknown. A recent report indicated that TCP9 modulates root system architectural plasticity in response to infections by the endoparasitic cyst nematode Heterodera schachtii via reactive oxygen species (ROS)-mediated processes in Arabidopsis, establishing a novel tolerance mechanism that mitigates the impact of biotic stress rather than targeting the causal agent [ 115 ].…”

“…MpTCP1 senses ROS levels and affects the expression of several enzymes involved in ROS metabolism, mediating adaptive responses to heat stress [ 13 ]. In Arabidopsis , TCP9 modulates ROS homeostasis in response to nematode infection [ 115 ] and class I TCP double and triple mutants exhibit enhanced ROS production [ 78 ]. It was also reported that expression of moso bamboo PeTCP10 increases drought tolerance in transgenic Arabidopsis via ROS-regulated root growth [ 120 , 121 ].…”

WOX11-mediated cell size control in Arabidopsis attenuates fecundity of endoparasitic cyst nematodes

“…However, previous research showed that the decreased ROS production in the rboh D/F mutant resulted in smaller syncytia and females compared to wild-type plants (Siddique et al ., 2014; Chopra et al ., 2021). While too high or too low levels of ROS can be deleterious for plants, modulation of ROS homeostasis within non-deleterious levels can regulate many cellular and physiological processes (Mittler, 2017, Willig et al ., 2022). For instance, modulation of ROS homeostasis via WOX11 could possibly mediate changes in syncytial cell wall extensibility in response to the fluctuations in sucrose and turgor pressure due to nematode cyclic feeding behavior.…”

From root to shoot; Quantifying nematode tolerance inArabidopsis thalianaby high-throughput phenotyping of plant development

“…For instance, a quantitative trait loci allele of ATS40-3 that was identified with a Genome Wide Association Study affects the sex ratio of H. schachtii in Arabidopsis (Anwer et al ., 2018). Recently, we also showed that the transcription factor TCP9 modulates tolerance to H. schachtii via reactive oxygen species mediated processes (Willig et al ., 2022). However, it remains unknown if A. thaliana harbours significant genetic variation in tolerance to nematodes.…”