Plant phenotyping for a sustainable future

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Several complex and interconnected megatrends such as climate change, environmental degradation, and stagnating yields threaten crop production and world food security for a growing global population (Maggio et al., 2018). This poses the challenge to develop sustainable and resilient agroecosystems with increased productivity as a key objective for the coming decades. In the past, agriculture has expanded production by breeding as well as by increasing inputs and farming areas. However, the projected scenarios call for considerable reductions in agricultural inputs such as water, fertilizers, and agrochemicals to reduce their environmental burden, whilst also addressing the decreasing land availability in many European countries. Integrated solutions and new technologies to improve plant production, based on knowledge-driven innovations in the farming sector and in agricultural and seed industries, have become the key objectives on the way towards sustainable agriculture (da Silva, 2015; Watt et al., 2020; Morisse et al., 2022). On average, and across all major arable crops cultivated in Europe, progress in breeding has contributed about 80% to overall productivity growth, based on genomic selection on yield but also, increasingly, on phenotypic traits that bring adaptations to environmental conditions, and that contribute to environmental and socio-economic benefits (Noleppa and Cartsburg, 2021). While genotyping efficiency is becoming increasingly rapid and its costs are declining, the extensive and growing genetic information obtained must be matched with quantitative analysis of crop performance with respect to structure, function, quality, and interaction within the environment; i.e. plant phenotyping. This has been recognised as being key in crop improvement and has been undergoing increasingly rapid development within the last decade, boosted mostly by new capabilities in process such as imaging and image analysis, automation, computing, and data analysis. This progress in phenotyping can be seen in the large increase in the number of publications from around 2010, with plant phenotyping increasingly being used to address a multitude of questions (Costa et al., 2019). Plant phenotyping has made substantial progress but still faces challenges that are inherent in the complexity and diversity of plants and traits, and the countless environmental scenarios that need to be quantified (Box 1). The functional body of the plant (‘Phenotype’) is formed during growth and development from the dynamic interactions between the genetic makeup (‘Genes’) and the physical world in which the plant develops (‘Environment’). These interactions determine plant performance and productivity, as measured by accumulated biomass and commercial yield, resource-use efficiency, and sustainability of plant production. Plant phenotyping is the process of quantitatively characterizing the structural and functional properties or traits of a phenotype within a dynamic environment. It represents an approach to delivering an integrated understanding of plant–environment interactions that can be translated into practical applications such as breeding or agronomy. Technological progress in hardware and software solutions has contributed to the advancement of plant phenotyping facilities and tools by increasing the use and application of non- or minimally invasive technology in automated modes that allows high-throughput assessment of a diversity of traits. Efforts have also been made in the development of affordable tools and approaches to meet the diverse needs of the research community, making plant phenotyping more accessible (Araus and Kefauver, 2018; Reynolds et al., 2019). It is important to remember that phenotyping is a rather complex tool and there is no one-size-fits-all solution. There is a large diversity of requirements to measure physiological and structural plant traits both above and below ground, from the level of tissues to plant to canopy, and from processes that occur over seconds in photosynthetic energy conversion to long-term processes such as growth and biomass accumulation—and all this in a dynamic biotic and abiotic environment. Hence, plant phenotyping will need to be continuously developed and adapted in order to address emerging questions, to deepen our knowledge of plant processes, and to help us to advance towards sustainable and resilient agriculture. Integrated concepts, technical solutions, and multi-scale methods and approaches are needed to fully exploit its potential. This cannot be effectively addressed at the institutional level or even within a single country. Therefore, integration of plant phenotyping efforts at national or regional levels is needed to enable plant scientists to better understand plant performance and to translate our knowledge into applications (see Pieruschka and Schurr, 2022). The International Plant Phenotyping Symposia initiated by the International Plant Phenotyping Network (IPPN; https://www.plant-phenotyping.org/) has been bringing the global plant phenotyping community together to exchange information and ideas, complemented by publication of the latest research in dedicated special issues in different journals (Pieruschka and Poorter, 2012; Pieruschka and Lawson, 2015; Reynolds and Schurr, 2019; Pommier et al., 2020). This current special issue continues the successful series of publications and has been stimulated by the Society of Experimental Biology virtual conference (SEB2021) and numerous activities initiated during the COVID-19 pandemic by the IPPN, the EU project EPPN2020, and by the plant phenotyping research infrastructure project EMPHASIS (https://emphasis.plant-phenotyping.eu/). This special issue addresses plant phenotyping as the key tool for understanding plant–environment interactions across different scales of resolution, from cellular to the whole plant (Janni et al., 2019). The reviews and research papers presented here highlight the ability of plant phenotyping to increase our understanding of plant performance and crop productivity and to improve it in terms of quality and tolerance to biotic and abiotic stresses. Climate change and the growing demand for food for both human and animal consumption during recent decades require ongoing development of climate-smart and resilient crops. Two review articles in this special issue present examples of how plant phenotyping can contribute to agricultural improvement. The Pannonian Plain has traditionally been a highly productive agricultural region in south-east Europe, with a high level of plant breeding and research playing an important role. Further advancement and implementation of phenotyping capacities will help us to explore the full potential of this region and further increase the agricultural productivity there (Kondic-Spika et al., 2022). The Nordic countries represent another region with very specific challenges with regards to crop cultivation, particularly because of the short growing season, long days, and the need for frost tolerance (Roitsch et al., 2022). Both regions are increasingly affected by climate change and there is a need for the development of adaptive capacity of crops that are both more climate resilient and perform well. Hence, regional strategies to implement phenotyping capacities in a coordinated way have been identified as being essential to effectively address the challenges and to utilize limited resources. Environmental stress can be diverse and affect plant productivity in different ways, and three reviews address different aspects of stress effects on plants. Pettenuzzo et al. (2022) describe the importance of understanding thermotolerance mechanisms in viticulture, and evaluate key traits with the aim of improving field management strategies and developing more resilient varieties. Waterlogging results in a different set of molecular and physiological responses, and presents an important challenge for plant phenotyping in Nordic countries (Langan et al., 2022). Profiling of the activities of key enzymes is emerging as a valuable tool to integrate cell physiological phenotyping into a functional phenomics approach to assess stress responses (Jammer et al., 2022). There is growing interest in the use of biostimulants as a tool for sustainable green economics in the agricultural context and how phenotyping can serve to identify new compounds and assess their biological activities and their mechanisms/modes of action (De Diego and Spìchal, 2022). Dedicated research papers complement these reviews by showcasing specific examples related to abiotic stress, including the resilience of wheat to high temperatures and drought (Correia et al., 2022), the responses of tomato to salinity, waterlogging, and elevated CO2 under controlled conditions (Zhou et al., 2022), the responses of rapeseed to waterlogging under field conditions (Li et al., 2022), the water-use efficiency of rice (Affortit et al., 2022), the combined nitrogen and water contents of lettuce (Weksler et al., 2022), the biotic interactions with root-associated microorganisms that stimulate growth and nutrient uptake in Brachypodium (Kuang et al., 2022), and the prediction of strawberry powdery mildew disease using spectral analysis of canopy reflectance combined with genomic information (Tapia et al., 2022). Plant phenotyping also provides data for the development of models. Aphalo and Sadras (2022) introduce a conceptual model linking developmental and evolutionary ecology with the acquisition of information through sensing of cues and signals that shows a multivariate complexity of the phenomics space and provides an explanation of pre-emptive acclimation. Additional models are also needed to improve the predictability of yield, and this issue is explored by Sarzaeim et al. (2022) in the use of climate data in crops such as maize. Overall, the range of contributions that form the core of this special issue show that plant phenotyping is becoming an increasingly important tool for many basic and applied questions in plant science, and integration of efforts is essential for further progress. Plant phenotyping has become an essential tool in disciplines such as breeding and precision farming, both under controlled conditions as well as in the field. Phenotyping can exploit advances in non-invasive sensor technology, machine learning, and robotics to improve efficiency, accuracy, and resolution. Further advancement of phenotyping towards sustainable plant production requires the integration of different elements. Phenotyping tools and technology have to be further developed and include environmental observations of diverse crops and traits of interests within dedicated facilities. Despite growing capacities and increasing throughput, plant phenotyping will never be able to measure all the plant–environment interactions experimentally, and hence harmonization is needed from experimental design to data acquisition and the reusability of data in models (Saint Cast et al., 2022). This will help us to identify the largest gaps in vitro and to address them experimentally in a targeted way, which will advance our knowledge of plant–environment interactions and hence contribute to improving our understanding of multiscale systems such as climate change, the transition of agriculture towards agroecology, and associated bioeconomic developments. Plant phenotyping has become a very cross-disciplinary research field, connecting the expertise of engineers, computer vision scientists, data scientists, plant scientists, and geneticists. An integration of effort is needed towards joint development and implementation of new hardware and software programs as well as data management and modeling capacities in order to be able to address the diversity of parameters such as crops, traits, and environmental conditions. Given the range of facilities, tools, and methods available, a coordinated approach is needed to effectively utilize limited resources. In particular, an integration of effort between scientists, organizations, and countries is needed to effectively address urgent questions related to sustainable agriculture. This will minimize duplication of efforts, and a coordinated approach will lead to a focus on the tools that are most needed and that will have the largest impact. An example of such an approach to integrate the community is the research infrastructure EMPHASIS, which aims at building a legal and scientific basis to coordinate and jointly advance the plant phenotyping and plant science community in Europe and beyond. This work was supported by the funding from the German Ministry of Education and Research BMBF funding DPPN under the Grant Agreement/FKZ 031B121, funding from the European Union’s Horizon 2020 program for the project EPPN2020 under Grant Agreement No. 731013, the project EOSC-Life under the Grant Agreement No. 824087, the project EMPHASIS-PREP under the Grant Agreement No. 739514, and the project RI-VIS under Grant Agreement No 824063. We greatly acknowledge the support of the International Plant Phenotyping Network, IPPN e.V.