**1. Introduction**

#### *1.1. Muscle Protein Metabolism and Skeletal Muscle*

The maintenance of and optimizing the accretion of skeletal muscle mass are critical outcomes for athletic-minded individuals, whether the goal is increased performance, improved muscularity, or enhanced recovery. Furthermore, while skeletal muscle mass accretion is often a goal of active individuals, there are direct clinical applications and benefits for the general public as well, especially for aging adults. Skeletal muscle is regulated through a near-continual ebb and flow between rates of muscle protein synthesis (MPS) and breakdown [1]. Muscle mass loss occurs during a net negative balance (breakdown > synthesis) while muscle gain occurs when synthesis rates outweigh breakdown. Rates of

**Citation:** Kerksick, C.M.; Jagim, A.; Hagele, A.; Jäger, R. Plant Proteins and Exercise: What Role Can Plant Proteins Have in Promoting Adaptations to Exercise? *Nutrients* **2021**, *13*, 1962. https://doi.org/ 10.3390/nu13061962

Academic Editor: David C. Nieman

Received: 24 April 2021 Accepted: 5 June 2021 Published: 7 June 2021

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**Copyright:** © 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https:// creativecommons.org/licenses/by/ 4.0/).

MPS and muscle protein breakdown are highly sensitive to physical activity and dietary intake, namely protein and essential amino acid intake [2], with evidence available indicating that rates of MPS are more sensitive to changes in exercise status and dietary intake [3]. As a result, observed changes in MPS rates are viewed to be primarily responsible for the changes in muscle mass in response to exercise and nutrition experienced over time [4].

#### *1.2. The Importance of Added Protein to Optimize Exercise Training Adaptations*

Supplementing the diet with added protein beyond the recommended dietary allowance (RDA) has long been a well-supported tactic for exercising athletes to optimize exercise training adaptations. In this respect, multiple review articles and position stands have advocated for a greater intake of dietary protein to support increased physical training volumes, heighten exercise training adaptations, and promote health and recovery [5–9]. Previously, Cermak and colleagues [10] completed a meta-analysis of studies that employed some form of protein supplementation while completing resistance training. Results from this analysis included data from over 680 subjects and concluded that protein supplementation led to a significantly greater increase in fat-free mass (mean difference: 0.69 kg, 95% CI: 0.47–0.91 kg, *p* < 0.001) and maximal lower-body strength (mean difference: 13.5 kg, 95% CI: 6.4–20.7 kg, *p* < 0.005) when compared to a placebo. These results were extended by Morton and investigators [7] who used a meta-analysis and meta-regression approach to establish the efficacy of protein supplementation while also identifying the minimum amount of daily protein needed to maximize efficacy. In this study, 49 studies were included that represented 1863 participants and the authors reported that protein supplementation was responsible for significant increases in strength (1 RM), fat-free mass, and muscle crosssectional area. Moreover, results from this study highlighted that a daily protein intake beyond 1.62 g/kg/day offered no further impact in facilitating improvements in fat-free mass. It is important to note, this is well above (~2×) the RDA for protein, indicating that active individuals benefit from consuming greater amounts of protein. Whether or not higher amounts facilitate improvements in other outcomes such as strength, recovery, mitigation of fat-free mass loss seen while dieting was not identified in their analysis. Notably, this amount of protein is consistent with the protein recommendation set forth by Jäger and colleagues [5] in the position stand published by the International Society of Sports Nutrition as well as the position stand endorsed by the American College of Sports Medicine, Dietitians of Canada and Academy of Nutrition and Dietetics (the former American Dietetic Association) [11]. Dietary proteins are well known to serve as the primary supplier of amino acids that can be used as building blocks to make larger proteins, such as those produced during MPS. Previous studies have highlighted the importance of the essential amino acids [12,13] at stimulating rates of MPS. In addition, extensive research continues to explore the role of leucine in its ability to stimulate the initiation of protein translation [14,15]. All things considered, exercising individuals require greater amounts of dietary protein to support their training needs, which creates a need for these individuals to purposefully include various sources of protein that deliver optimal amounts of the essential amino acids.

#### *1.3. The Case for Plant Proteins*

Many sources of protein are available for consumption in the human diet. For years, heavy emphasis was placed on consuming complete protein sources, or any protein source that provides all of the essential amino acids in both the needed amount and in adequate proportion to support cellular needs across the body as well as production of nonessential amino acids [8]. Consequently, grea<sup>t</sup> focus has been placed on consuming animal protein sources, namely because of their high amino acid contents and favorable protein quality ratings [16]. At the same time, plant proteins were deemed inferior for these outcomes and not until recently has interest in plant proteins begun to accelerate. Several reasons are commonly associated with consuming greater amounts of plant proteins. Most commonly, plant-based diets are routinely linked with reductions in the risk of developing cancers, type

2 diabetes, and cardiovascular diseases [17]. In addition, many plant protein advocates highlight a greater level of economic sustainability than what is observed with diets that are predominantly animal protein. Finally, approximately 60% of dietary proteins consumed worldwide come from plant sources with an estimated 4 billion people across the globe consuming a primarily plant-based diet [18]. While such health considerations are unquestionably important, the aim of this review will center upon the implications of plant protein consumption and plant-based diets on outcomes linked to exercise performance, associated exercise training adaptations, and recovery.

#### *1.4. Quality Considerations for Both Animal and Plant-Based Protein*

Many factors contribute to the anabolic potential of a protein source, which often include the amounts of total amino acids, essential amino acids, and branched-chain amino acids, respectively in addition to the protein's digestibility, digestion rate, and kinetics observed during absorption. In this respect, dietary protein quality is commonly assessed based upon the essential amino acid composition provided by the protein source as it relates to human needs, against the ability of the protein to be digested, absorbed, and assimilated by various tissues in the body [19]. Several approaches have been used to assess protein quality including biological value, net protein utilization, and protein digestibility corrected amino acid scores (PDCAAS) [20], while digestible indispensable amino acid score (DIAAS) have been more recently proposed. As seen in an excellent review by Berrazaga et al. [16], biological values for common plant sources range from 56–74 while ranges of 77–104 are reported for various animal sources on theoretical 100-point scales. A similar dichotomy is observed for net protein utilization values, whereby plant sources range from 53–67 while animal sources range from 73–94 on a 100-point scale. One of the most commonly used quality comparators is that of Protein Digestibility Corrected Amino Acid Scores (PDCAAS) [21]. When using this approach, a score of 100 suggests that after considering its fecal digestibility, a given protein source can fully deliver all of the essential amino acids required by the body. In this respect, animal protein sources such as casein, whey, milk, and eggs all have scores of 100 while red meat has a score of 92. In contrast, all other common sources of plant proteins have PDCAAS values below 100 (commonly reported range of 45–75 per Barrazaga et al. [16]), with soy protein being the only exception, which has a score of 100. Similarly, if the DIAAS approach is used to assess protein quality, a similar trend is observed in that animal sources are commonly above 100 while nearly all plant sources are below 100. In this respect, Gorissen et al. [22] compared the amino acid contents of various sources of plant-based isolates against common sources of animal proteins and human skeletal muscle samples. Again, it was illustrated that many plant protein sources have inadequate amounts of certain amino acids (e.g., lysine, methionine) while also consistently having lower amounts of the essential and branchedchain amino acids, particularly when compared to animal protein sources as well as the amino acid content found in human skeletal muscle. To further reiterate this point, van Vliet and colleagues [23] have indicated previously that essential amino acid composition of a protein source was predictive of skeletal muscle's anabolic potential and that all essential amino acids should be present in optimal amounts. For these reasons, higher quality sources of protein (at least when viewed in the context of amino acid profiles) should serve as more effective protein sources in terms of anabolic potential and its innate ability to facilitate skeletal muscle accretion and promote other desired adaptations. Finally, leucine content of a protein source continues to ge<sup>t</sup> interest for its role in initiating the translation of muscle proteins [14,15]. Towards this end, a general acceptance has suggested the leucine content of a protein source functions as a vital and reliable predictor of MPS rates. When leucine contents are compared across different protein sources, whey protein is the highest (~12–14%) [22], which aligns with whey protein's superior ability to stimulate MPS rates when compared to isocaloric and isonitrogenous amounts of other protein sources [24]. Moreover, animal protein sources generally have higher amounts of leucine (8–9% for

non-dairy animal sources) and >10% for dairy protein sources while plant sources routinely have a leucine content of 6–8% [22,23].

Beyond amino acid content, digestibility and absorption kinetics can also influence the value of a protein. In terms of digestibility, it is well documented that the digestibility of many sources of plants is much lower (45–80%) than what is observed with various animal proteins (>90%) [25]. While somewhat beyond the scope of this review, the observed differences in digestibility are largely thought to be due to structural differences that exist within the actual protein molecule found in many plant and animal proteins. For example, many sources of plants have compounds (i.e., anti-nutritional factors such as phytic acid, protease inhibitors, tannins, etc.) that compromise their digestibility. Another key factor related to the impact of consuming different sources of protein is the absorption of amino acids in plasma followed by the utilization rates exhibited by various proteins. In this respect, several studies have illustrated divergent utilization rates when comparing animal to plant sources of protein. For example, the classic work of Boirie [26,27] and Dangin [28,29] clearly demonstrated different absorption and utilization rates for two milk proteins, whey and casein. Moreover, the observed differences in rates of muscle protein metabolism have been shown to be inextricably linked to differences in utilization rates whereby whey absorbs faster and robustly stimulates rates of MPS while casein absorbs at a slower rate and consequently functions more to attenuate protein breakdown. When considering differences observed for various plant proteins, previous work has shown that soy ingestion is absorbed at a slower rate than what is observed from whey [24,30], which helps to explain the lower rates of myofibrillar protein synthesis observed by Yang and colleagues [4] after graded doses (0–40 g) of soy isolate at rest and after exercise in elderly men. While rates of myofibrillar protein synthesis were observed to increase with an increase in the dose of soy protein, the observed rates were less than what had been previously observed with equivalent doses of whey [24]. Additional research involving wheat proteins demonstrated them to have higher deamination rates when compared to milk proteins (25% vs. 16%, respectively) [31–33]. These differences are important as they are thought to be directly related to the lower observed net protein utilization rates between wheat (66%) when compared to milk (80%) proteins. Furthermore, other studies have illustrated a greater degradation of amino acids from soy protein when compared to degradation rates observed for casein and whey [24,30,34,35]. Towards this end, measured nitrogen losses (either via deamination or intestinal loss) and splanchnic nitrogen retention are higher when plant proteins are consumed when compared to ingestion of animal proteins. In effect, these outcomes illustrate that the availability of amino acids to peripheral tissues and locations from plant proteins is lower than that of animal protein [36,37] and these differences are thought to be key drivers to the post-prandial protein synthetic response observed in various tissues. Importantly, the reader should understand that these reasons effectively function as the basis for why different sources of protein exhibit varying degrees of anabolic potential, in regards to stimulating muscle protein accretion and promotion of exercise training adaptations over time.
