Non-technical summary: Modern agriculture is associated with numerous environmental predicaments, such as land degradation, water pollution, and greenhouse gas emission. Socio-economically, it is characterized by a treadmill of technological change, increased mechanization, and economic consolidation, while depressing economic returns to farmers. A root cause is the dominance of annual plants cultivated in monocultures. Annual crops require the yearly clearing of vegetation resulting in soil erosion and other forms of ecosystem degradation. Monocultures are susceptible to agricultural pests and weeds. By contrast, perennial polycultures informed by natural ecosystems, promise more sustainable agroecosystems with the potential to also revitalize the economic foundation of farming and hence rural societies.

Over the last century, researchers and practitioners with diverse backgrounds have articulated the importance of improving soil organic matter (SOM) contents in agricultural soils. More recently, climate change scientists interested in CO₂ sinks, and agroecologists interested in ecological intensification have converged on the goal of building SOM stocks in croplands. The challenge is that agriculture itself is responsible for dramatic losses of SOM. When grassland or forest ecosystems are first converted to agriculture, multiple mechanisms result in SOM declines of between 20% and 70%. Two of the most important mechanisms are the reduction in organic matter inputs from roots following the replacement of perennial vegetation with annual crop species, and increases in microbial respiration when tillage breaks open soil aggregates exposing previously protected organic matter. Many agricultural practices such as conservation tillage and integration of cover crops have been shown to achieve some degree of SOM improvement, but in general adoption of these practices falls short of accumulating the SOM stocks maintained by grasslands, forests or other native ecosystems that agriculture replaced. Two of the overarching reasons why native terrestrial ecosystems have achieved greater soil organic matter levels than human agroecosystems are because they direct a greater percentage of productivity belowground in perennial roots, and they do not require frequent soil disturbance. A growing body of research including that presented in this review suggests that developing perennial grain agroecosystems may hold the greatest promise for agriculture to approach the SOM levels that accumulate in native ecosystems. We present calculations that estimate potential soil organic carbon accumulation rates in fields converted from annual to perennial grains of between 0.13 and 1.70 t ha⁻¹ year⁻¹.

The development of new perennial crop species is gaining momentum as a promising approach to change the fundamental nature of ecosystem processes in agriculture. The ecological argument for perennial crops grown in polycultures is strong, but until recently, perennial herbaceous grain crops have been absent from agricultural landscape. This is not because perennial herbaceous species do not exist in nature—there are thousands of perennial grasses, legumes, and other broad leaf plants. Rather, for a variety of reasons, early farmers focused on cultivating and domesticating annuals, and the perennial herbs were largely ignored. Today, we have a tremendous opportunity to explore another agricultural path. Building on contemporary knowledge of plant biology and genetics that early farmers lacked, and using a rapidly expanding toolbox that includes sophisticated genomic and analytical approaches, we can develop viable perennial grain crops. These crops can then be used to assemble diverse agroecosystems that regenerate soils and capture other important ecosystem functions.

Silflower (Silphium integrifolium Michx.) is in the early stages of domestication as a perennial version of oilseed sunflower, its close relative. Grain crops with deep perennial root systems will provide farmers with new alternatives for managing soil moisture and limiting or remediating soil erosion, fertilizer leaching, and loss of soil biota. Several cycles of selection for increased seed production potential following initial germplasm evaluation in 2002 have provided opportunities to document the botany and ecology of this relatively obscure species, to compare agronomic practices for improving its propagation and management, and to evaluate the differences between semi-domesticated and wild accessions that have accrued over this time through intentional and unintentional genetic processes. Key findings include: domestication has increased aboveground biomass at seedling and adult stages; seed yield has increased more, achieving modest improvement in harvest index. Harvest index decreases with nitrogen fertilization. Silflower acquires nitrogen and water from greater depth than typical crops. In agricultural silflower stands within its native range, we found that Puccinia silphii (rust) and Eucosma giganteana (moth) populations build up to unacceptable levels, but we also found genetic variation for traits contributing to resistance or tolerance. Breeding or management for reduced height and vegetative plasticity should be top priorities for future silflower research outside its native range.

This article was written as a response to Chris Smaje’s review, “The Strong Perennial Vision: A Critical Review” [this issue]. In his review, Smaje argues that society in general, and the research community in particular should question whether to invest substantially in the development of perennial grains because a) ecological theory suggests that perennial grains may yield less than annual grains; b) strong criticisms of annual agriculture are unfounded, both socially and ecologically; and c) focus on perennial grains detracts from more important strategies for achieving agricultural sustainability. We counter these three arguments by showing a) that Grime’s C-S-R theory employed by Smaje is not meaningful when used to predict the “evolvability” of perennial species under selection in agricultural environments; b) that annual grain ecosystems have not broadly achieved an acceptable level of ecosystem function or resilience; and c) that perennial grain research is not currently attracting the attention or resources that other, less promising and less transformative research efforts garner.