Plant trait diversity is known to influence population yield, but the scale at which this happens remains unknown: divergent individuals might change yields of immediate neighbors (neighbor scale) or of plants across a population (population scale). We use Nicotiana attenuata plants silenced in mitogen-activated protein kinase 4 (irMPK4) - with low water-use efficiency (WUE) - to study the scale at which water-use traits alter intraspecific population yields. In the field and glasshouse, we observed overyielding in populations with low percentages of irMPK4 plants, unrelated to water-use phenotypes. Paired-plant experiments excluded the occurrence of overyielding effects at the neighbor scale. Experimentally altering field arbuscular mycorrhizal fungal associations by silencing the Sym-pathway gene NaCCaMK did not affect reproductive overyielding, implicating an effect independent of belowground AMF interactions. Additionally, micro-grafting experiments revealed dependence on shoot-expressed MPK4 for N. attenuata to vary its yield per neighbor presence. We find that variation in a single gene, MPK4, is responsible for population overyielding through a mechanism, independent of irMPK4's WUE phenotype, at the aboveground, population scale.
Keywords: N. attenuata; arbuscular mycorrhizal fungi; ecology; field; mitogen-activated protein kinase 4; plant biology; scale; water-use efficiency.
Whether on farmland or in a forest, plants do not grow in isolation. Plants compete with their neighbors over limited space and resources, and individual plants respond to this competition in different ways by changing how much they grow and how they use resources. The efficiency with which crop plants use water, for example, is one trait that is dramatically influenced by neighboring plants and is of increasing concern given the warming climate. Understanding the effects of interactions between individual plants in a population as a whole is complicated, especially in natural plant communities where neighbors are often from different species. For this reason, McGale et al. took a different approach and looked at neighbors that were all from the same species and differed only in the activity of a single gene. The species in question was coyote tobacco, a plant that is native to western North America. McGale et al. used genetic engineering to silence a gene called MPK4, which was known from previous studies to have the effect of reducing water-use efficiency. Some of these ‘water-inefficient’ plants were then grown in mixed populations with plants that had normal levels of MPK4. In experiments conducted both in a glasshouse and at a field station in the Utah desert, McGale et al. found that populations with a low percentage of the MPK4-silenced plants were actually more productive than ‘monocultures’ that were all one type or the other. Further analysis showed that the increase in productivity did not depend on the different soil nutrient or water use of the different populations, or even the density of the plants in the populations. Pairs of plants grown in single pots essentially ruled out any interactions between immediate neighbors being responsible for the increased productivity, suggesting that that effect must instead emerge at the level of the population. Perhaps unexpectedly, McGale et al. also found that the MPK4-silenced plants and control plants did not actually differ in how they used water when grown in the field (previous studies had all been conducted in glasshouses), indicating that this trait also could not explain the observed population-level effect. Finally, experiments that involved grafting the shoots of one plant onto the roots of another suggested that the effect most likely comes from the aboveground parts of the plant. Ecologists have previously noted that more diverse populations typically have higher productivity. This new finding that a small percentage of slightly different plants in an otherwise uniform population can increase overall productivity will likely to be of special interest to researchers looking to boost the efficiency of agricultural ecosystems. Also, since MPK4 is highly conserved, and thus likely to be found in many plant species, this could be an interesting trait with which to study the interactions of natural plant communities.
© 2020, McGale et al.