Activation of seminal root primordia during wheat domestication reveals underlying mechanisms of plant resilience

Abstract

Seminal roots constitute the initial wheat root system and provide the main route for water absorption during early stages of development. Seminal root number (SRN) varies among species. However, the mechanisms through which SRN is controlled and in turn contribute to environmental adaptation are poorly understood. Here, we show that SRN increased upon wheat domestication from 3 to 5 due to the activation of 2 root primordia that are suppressed in wild wheat, a trait controlled by loci expressed in the germinating embryo. Suppression of root primordia did not limit water uptake, indicating that 3 seminal roots is adequate to maintain growth during seedling development. The persistence of roots at their primordial state promoted seedling recovery from water stress through reactivation of suppressed primordia upon rehydration. Our findings suggest that under well-watered conditions, SRN is not a limiting factor, and excessive number of roots may be costly and maladaptive. Following water stress, lack of substantial root system suppresses growth and rapid recovery of the root system is essential for seedling recovery. This study underscores SRN as key adaptive trait that was reshaped upon domestication. The maintenance of roots at their primordial state during seedling development may be regarded as seedling protective mechanism against water stress.

Domestication and crop evolution of wheat and barley: Genes, genomics, and future directions

“…Unlike the above ground part of plants, the root system is not well studied; nevertheless, the roots are equally important to the plant for anchoring the plant and nutrient uptake (Osmont et al ). One study, in particular, elegantly demonstrated that the number of seminal roots increased from three to five as a result of wheat domestication (Golan et al ). These authors showed that, in wild wheat, two root primordia are suppressed at the embryonic stage as an adaptive purpose, allowing the plants to respond to drought at early growth stages.…”

Characterization of root traits for improvement of spring wheat in the Pacific Northwest

“…In the field, root growth can be severely arrested due to edaphic constraints such as extreme drought (Richards et al, 2010), and root systems exhibit a substantial degree of phenotypic plasticity in response to environmental cues (Kano, Inukai, Kitano, & Yamauchi, 2011;Osmont et al, 2007;Palmer, Bush, & Maloof, 2012). In fact, Hollis and Drysdale did not differ significantly in dryland farming conditions in terms of root number, length, and volume in field settings (Ghimire, 2017). Nonetheless, the genetic variability identified in this research, and knowledge gained from these studies can be leveraged to develop drought-resilient wheat cultivars with improved root systems through molecular and quantitative genetic approaches (de Dorlodot et al, 2007;Watt et al, 2013a) targeting dryland farming communities, particularly in the face of global climate change (IPCC, 2014).…”

“…The results from early growth of seminal roots is important for the implication of seedling root traits for both plant establishment and the relation to dynamic root functions as plants grow and mature (Golan, Hendel, Méndez Espitia, Schwartz, & Peleg, ). The seminal roots and their laterals also contribute significantly to form the bulk of the fibrous wheat root system (Osmont, Sibout, & Hardtke, ) which have been subjected to selection pressure during crop domestication for promoting seedling recovery against drought stress (Golan et al., ). On average, the spring wheat cultivars produced 1.2‐cm seminal root growth per day across the 5‐d study period (data not shown) which was similar to the 1–3 cm of primary (seminal) axile root elongation of wheat seedlings observed in a paper roll experiment (Watt et al., ).…”

Genetic screening for mutants with altered seminal root numbers in hexaploid wheat using a high-throughput root phenotyping platform

“…This likely suggests that the developments of the different seminal root types are under distinct genetic control, with SR 1 and SR 2,3 being more conserved than SR 4,5 and SR 6 . This notion is supported by reports that SR 4,5 show only negligible contribution to water uptake and does not confer any beneficial fitness under well-watered conditions (Golan et al 2018). It is however possible that SR 4,5 and indeed SR 6 may contribute significantly to nutrient and water uptake under resourcelimiting conditions where increase in root surface area maximises soil exploration.…”

“…They have been shown to have similar nutrient uptake efficiency as nodal roots in wheat (Kuhlmann and Barraclough 1987) and contribute to yield potential especially under conditions of low soil moisture where nodal roots may not grow (Weaver and Zink 1945;Sanguineti et al 2007;Sebastian et al 2016). Given their importance, seminal root traits, angle and number, have been linked to adaptive responses under water limiting conditions (Manschadi et al 2008;Cane et al 2014;Golan et al 2018). Steep seminal root angle has been associated with the increased soil water exploration at depth beneficial in drought condition where topsoil moisture is depleted (Richard et al 2015;Olivares-Villegas et al 2007;Manschadi et al 2008).…”