Wild Cicer species exhibit superior leaf photosynthetic phosphorus- and water-use efficiencies compared with cultivated chickpea under low-phosphorus conditions

Abstract

Introduction

Chickpea (Cicer arietinum) is a vital legume crop for food and feed in developing countries (Foyer et al., 2016). However, domestication has significantly narrowed its genetic diversity (Abbo et al., 2003; Varshney et al., 2013, 2021; Marques et al., 2020; Khan et al., 2024). To address this limitation, the International Crops Research Institute for the Semi-Arid Tropics (ICRISAT) developed a chickpea reference set of 300 accessions from 29 countries, representing diverse genetic backgrounds (Upadhyaya et al., 2008). Studies on this set revealed significant genotypic variation in plant growth, shoot phosphorus (P) content, physiological P-use efficiency (PUE), leaf photosynthetic characteristics, photosynthetic PUE (PPUE), root morphology, carboxylate exudation, and arbuscular mycorrhizal fungal colonisation (Pang et al., 2018a,b, 2023; Wen et al., 2020, 2022). However, this reference set included only seven wild Cicer accessions due to the limited global collections available at the time (Berger et al., 2003; Coyne et al., 2020). Wild species are typically genetically much more diverse than their domesticated counterparts due to the domestication bottleneck (Tanksley & McCouch, 1997; Purugganan & Fuller, 2009). While crops are weak competitors in managed systems that minimize stress, wild progenitors such as wild Cicer thrive in unregulated low-fertility environments (Renzi et al., 2022). Therefore, screening wild germplasm for nutrient acquisition capacity is crucial. Recent international collaborations have expanded wild Cicer collections (von Wettberg et al., 2018), enabling exploration of their genetic diversity for abiotic stress tolerance, including low P availability.

Cicer reticulatum, the primary gene pool of cultivated chickpea, is fully compatible with domesticated C. arietinum (Coyne et al., 2020). The secondary gene pool, C. echinospermum, exhibits variable compatibility with cultivated chickpea depending on the population (Kahraman et al., 2017). Both wild species are restricted to south-eastern Anatolia, Türkiye, where they inhabit distinct ecological niches shaped by diverse soil substrates and a steep elevational gradient exceeding 1000 m (von Wettberg et al., 2018). Therefore, localized adaptation underscores their potential for broadening the genetic base of chickpea and introducing adaptive traits lost during domestication (Croser et al., 2003; von Wettberg et al., 2018).

Recent studies have explored wild Cicer species for genotypic variation under abiotic stress, such as heat (von Wettberg et al., 2018), drought (von Wettberg et al., 2018; Berger et al., 2020), nitrogen (N) deficiency (Marques et al., 2020), and aluminium toxicity (Vance et al., 2021), biotic stress like Helicoverpa armigera infestation (von Wettberg et al., 2018), and seed quality traits, including nutrient composition (von Wettberg et al., 2018; Sharma et al., 2021) and seed size (von Wettberg et al., 2018). Given that wild Cicer species naturally inhabit low-P soils, they may possess traits for greater P-use efficiency.

Phosphorus availability often limits crop production, with up to 80% of applied P fertilizer rendered unavailable to plants due to its conversion into insoluble complexes in acidic and alkaline soils (Raghothama, 1999; Lambers, 2022). Enhancing PUE, defined as increased yield per unit P applied, is an environmentally sustainable strategy (Rose et al., 2013). PPUE, the photosynthesis rate per unit of leaf P, is a critical component of PUE, given that photosynthesis contributes over 90% of crop biomass (Veneklaas et al., 2012; Cong et al., 2020). Despite its importance, few studies have examined the effects of domestication on PUE, particularly PPUE in crops, including the chickpea breeding programme (Chen et al., 2024; Wang et al., 2024). Previous research demonstrated significant genotypic variation in PUE, including P-acquisition efficiency, physiological PUE, and PPUE among domesticated C. arietinum accessions under low-P conditions (Pang et al., 2018b) and revealed biochemical mechanisms underpinning a high PPUE, such as a different allocation to foliar P fractions, with a lower allocation to Pi and metabolite P but a greater allocation to nucleic acid P (Wen et al., 2022). However, the genetic diversity of P acquisition and PPUE in the genus Cicer remains unexamined, particularly among wild Cicer accessions.

Domestication effects on leaf gas exchange traits vary among crops. For instance, Milla & Matesanz (2017) reported reduced photosynthesis rates during the domestication of Beta vulgaris, Helianthus annuus, Solanum lycopersicum, and Zea mays. Conversely, studies have shown an increased photosynthesis rate in domesticated crops compared with their wild relatives, such as chickpea under both N-deficient and N-sufficient conditions (Marques et al., 2020), cotton (Gossypium hirsutum) (Z. Y. Lei et al., 2023), and soybean (Glycine max) (Chen et al., 2024; Pelech et al., 2025). Recently, Lei et al. (2024) reported stage-specific increases in photosynthesis rate during domestication, influenced by variation in light intensity. The transition from wild to semiwild accessions resulted in a faster photosynthesis rate and lower leaf mass per area (LMA) under high light intensity, whereas the transition from semiwild to domesticated accessions enhanced photosynthesis under low light intensity. Whether domestication similarly affects leaf gas exchange in Cicer grown under sufficient light intensity, particularly under low-P conditions, is unknown.

Wild species and their relatives generally exhibit thicker leaves and higher LMA than their domesticated counterparts, as observed in Cicer (Marques et al., 2020) and Gossypium (Lei et al., 2021; Z. Y. Lei et al., 2023). Higher LMA is often associated with resilience to drought by reducing wilting risk (Wright et al., 2001). However, a trade-off between water-use efficiency (WUE) and photosynthetic N-use efficiency (PNUE) has been documented in noncrop plants (Field et al., 1983; Wright et al., 2001; Zhou et al., 2024) as well as in Triticum aestivum (Van Den Boogaard et al., 1997). For example, dry-site tree species maintain area-based photosynthesis rates with lower stomatal conductance by increasing leaf N concentrations, thus minimising water loss (Wright et al., 2001). Whether this trade-off exists among Cicer species, particularly under low-P conditions, remains unknown.

In this study, we used the wild Cicer collection to evaluate vegetative growth, photosynthesis characteristics, PPUE, and PNUE under low-P conditions. We hypothesized that: (1) significant variation in leaf gas exchange and PUE exists among wild Cicer accessions due to their distinct natural habitats; (2) variation among wild Cicer accessions exceeds that in cultivated C. arietinum; (3) wild Cicer species exhibit greater PPUE than domesticated chickpea; and (4) wild Cicer species display a trade-off between higher instantaneous intrinsic WUE and lower PNUE.