Balance under Stress: A Case of Mixed Signals

Plants may appear to be sitting ducks to whatever pest, pathogen, or bad weather assaults them, but they are far from defenseless. In fact, plants are artful masters of war, armed with elaborate physical and chemical defense systems. But, in many cases, optimizing growth and defense is like running a business or a laboratory on a budget. A plant has a certain amount of resources that may be expended on the production of vegetative and reproductive tissues as well as physical barriers and defense compounds (Züst and Agrawal, 2017). To successfully manage all these activities, plants must acquire adequate resources to fund them.

Both excess or shortage of resources, such as potassium or nitrogen (N), can lead to the overproduction of reactive oxygen species (ROS; Shin and Schachtman, 2004; Shin et al., 2005), which wreak havoc on cellular membranes, proteins, and DNA (Møller et al., 2007). To minimize the damage from and, if possible, escape the source, plants must properly perceive, diagnose, and respond to the stress. As we rely on plants for myriad essential resources, including food, medicine, fuel, soil stabilization, shelter, and clothing, unraveling the intricate processes plants use to perceive and respond to various stresses may help us optimize crop yield under stressful conditions.

Plant mutants are useful tools for discovering key elements of stress response pathways. In this issue of Plant Physiology, Bellegarde et al. (2019) investigate the role of a modifier protein called HIGH NITROGEN INSENSITIVE9 (HNI9) in alleviating stress caused by excess N (Bellegarde et al., 2019). They started with the observation that hni9-1 mutant plants have increased expression of the nitrate transporter NRT2.1 when N is abundant. In wild-type Arabidopsis (Arabidopsis thaliana) plants, NRT2.1 is up-regulated in response to N starvation to promote the production of lateral roots to hunt down the limiting nutrient and to actively import N into the roots (Remans et al., 2006; Fig. 1). Inducing NRT2.1 under excess N conditions is the exact opposite of the desired response, revealing that hni9-1 mutant plants somehow have their signals crossed. So, what exactly is the connection between NRT2.1 and HNI9?

Figure 1.

HNI9 and HY5 initiate a detoxification response to maintain ROS homeostasis under excess N conditions. When N is limiting (left side), ROS (pink stars) accumulate, leading to NRT2.1 induction. NRT2.1 promotes lateral root growth and increases import of N into the roots to alleviate stress associated with N starvation. When N is in excess (right side), HNI9 increases the H3K4me3 active chromatin mark to prime expression of a suite of detoxification genes. HY5 then acts as a master regulator to promote the transcription of these genes to maintain ROS homeostasis. Figure made in ©BioRender (biorender.com).

HNI9 is a modifying factor of chromatin, which is a combination of DNA and its protein packaging. Just like football coaches use images or signals to call plays from the sideline, chromatin modifiers use specific marks to make genes open or closed for expression. Bellegarde et al. (2019) show that, in response to excess N, HNI9 tags a suite of detoxification genes with a specific active chromatin mark. Then, the transcription factor, HY5, acts as the quarterback, or master regulator, to ensure that these genes are expressed. As a result, ROS homeostasis is maintained, thereby preventing the misregulation of NRT2.1 (Fig. 1). Since HY5 induces NRT2.1 expression in the roots under other circumstances (Chen et al., 2016), it is critical that HNI9 properly mark the DNA so HY5 activates the appropriate set of genes. If either HNI9 or HY5 is inactivated under excess N conditions, the right DNA marks are not made or there is no regulator to act on them. This leads to ROS overaccumulation, NRT2.1 induction, and stunted primary root growth.

Bellegarde et al. (2019) also show that ROS-generating compounds induce NRT2.1 in wild-type plants, indicating that both loss of HNI9 negative regulation (Widiez et al., 2011) and ROS overaccumulation may contribute to NRT2.1 induction under high-N conditions in hni9-1 mutants. As elevated ROS occurs in wild-type plants under N starvation (Shin et al., 2005), this may be an important trigger to appropriately induce NRT2.1 to deal with that stress.

Depending on the stress severity, the potential outcomes for incorrect responses to stressful situations are deficiencies in growth, development, and reproduction or possibly plant death. By identifying key players involved in maintaining ROS homeostasis in response to excess N, Bellegarde et al. (2019) have deepened our understanding of one of the plant’s many complex stress response pathways, moving us one step closer to our goal of maximizing plant growth and yield under suboptimal conditions.