TaER Expression Is Associated with Transpiration Efficiency Traits and Yield in Bread Wheat

RESEARCH ARTICLE TaER Expression Is Associated with Transpiration Efficiency Traits and Yield in Bread Wheat Jiacheng Zheng1, Zhiyuan Yang1, Pippa J. Madgwick2, Elizabete Carmo-Silva2, Martin A. J. Parry2*, Yin-Gang Hu1,3* a11111 1 State Key Laboratory of Crop Stress Biology for Arid Areas and College of Agronomy, Northwest A&F University, Yangling, Shaanxi, China, 2 Department of Plant Biology and Crop Science, Rothamsted Research, Harpenden, Hertfordshire, United Kingdom, 3 Institute of Water Saving Agriculture in Arid Regions of China, Yangling, Shaanxi, China * (MP); (YGH) Abstract OPEN ACCESS Citation: Zheng J, Yang Z, Madgwick PJ, CarmoSilva E, Parry MAJ, Hu Y-G (2015) TaER Expression Is Associated with Transpiration Efficiency Traits and Yield in Bread Wheat. PLoS ONE 10(6): e0128415. doi:10.1371/journal.pone.0128415 Academic Editor: Wujun Ma, Murdoch University, AUSTRALIA Received: February 10, 2015 Accepted: April 27, 2015 Published: June 5, 2015 Copyright: © 2015 Zheng et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper and its Supporting Information files. Funding: This work was supported by the subproject of the 863 Program (2013AA102902) of the Ministry of Science and Technology, and the China 111 Project (B12007), P. R. China. Jia-Cheng Zheng was supported by a Joint PhD scholarship of the Chinese Scholarship Council. Pippa Madgwick, Elizabete Carmo-Silva and Martin Parry acknowledge financial support from the BBSRC 20:20 Wheat Institute Strategic Programme (BBSRC BB/J/00426X/ 1). ERECTA encodes a receptor-like kinase and is proposed as a candidate for determining transpiration efficiency of plants. Two genes homologous to ERECTA in Arabidopsis were identified on chromosomes 6 (TaER2) and 7 (TaER1) of bread wheat (Triticum aestivum L.), with copies of each gene on the A, B and D genomes of wheat. Similar expression patterns were observed for TaER1 and TaER2 with relatively higher expression of TaER1 in flag leaves of wheat at heading (Z55) and grain-filling (Z73) stages. Significant variations were found in the expression levels of both TaER1 and TaER2 in the flag leaves at both growth stages among 48 diverse bread wheat varieties. Based on the expression of TaER1 and TaER2, the 48 wheat varieties could be classified into three groups having high (5 varieties), medium (27 varieties) and low (16 varieties) levels of TaER expression. Significant differences were also observed between the three groups varying for TaER expression for several transpiration efficiency (TE)- related traits, including stomatal density (SD), transpiration rate, photosynthetic rate (A), instant water use efficiency (WUEi) and carbon isotope discrimination (CID), and yield traits of biomass production plant-1 (BYPP) and grain yield plant-1 (GYPP). Correlation analysis revealed that the expression of TaER1 and TaER2 at the two growth stages was significantly and negatively associated with SD (P<0.01), transpiration rate (P<0.05) and CID (P<0.01), while significantly and positively correlated with flag leaf area (FLA, P<0.01), A (P<0.05), WUEi (P<0.05), BYPP (P<0.01) and GYPP (P<0.01), with stronger correlations for TaER1 than TaER2 and at grain-filling stage than at heading stage. These combined results suggested that TaER involved in development of transpiration efficiency -related traits and yield in bread wheat, implying a function for TaER in regulating leaf development of bread wheat and contributing to expression of these traits. Moreover, the results indicate that TaER could be exploitable for manipulating important agronomical traits in wheat improvement. PLOS ONE | DOI:10.1371/journal.pone.0128415 June 5, 2015 1 / 17 TaER Expression Associated with TE Traits and Yield Competing Interests: The authors have declared that no competing interests exist. Introduction In many regions of the world, water deficits impose serious constraint on plant growth and crop productivity. Plant transpiration efficiency (TE) is critical to plant survival and has important implications for both carbon cycling and water balance. Plants have evolved a variety of ways of controlling TE; understanding this control is essential to underpin attempts to improve crop productivity with limited water availability. TE is affected significantly and variably by canopy characteristics and leaf anatomy (i.e. leaf thickness, mesophyll cell size and position, stomatal density) and activity (stomatal conductance). In Arabidopsis thaliana, ERECTA (ER) was demonstrated to regulate the development of leaf architecture, and be a major gene contributing to TE, ER was the major contributor to a locus for carbon isotopic discrimination (Δ) and was negatively related to transpiration efficiency [1]. Thus, understanding the ER genotypic variation of leaf traits will be valuable to in attempts to improve TE, photosynthesis and crop productivity. ER is associated with numerous functions that affect plant development and TE [2]. The ER gene was first isolated from Arabidopsis thaliana and belongs to the receptor-like kinase family (RLKs) with an N-terminal extracellular domain and C-terminal intracellular kinase that transduces extracellular signals into the cells to control a wide range of physiological responses [3, 4, 5]. The role of ER has been examined by both forward and reverse genetic approaches. Mutations to ER in Arabidopsis conferred decreased TE, but ER complementation led to restoration of TE [1]. In transgenic tomato plants, the expression of a truncated ER protein from Arabidopsis (atΔKinase), increased the number of stomata per leaf, transpiration and photosynthetic rates [6]. Over-expression in Arabidopsis of the PdERECTA gene from Populus nigra L. (35S: PdERECTA) increased photosynthetic rate, whilst decreasing transpiration rate and thereby increasing water use efficiency (WUEi) [7]. Complete function loss of three ER-family genes (ER, ER-LIKE1 (ERL1) and ERL2) in Arabidopsis resulted in the generation of high-density stomatal clusters and a 50–200% increase of the stomatal index [8]. ER appears to play a central role in the epidermal cell differentiation signaling pathway, inhibiting stomatal development and leading to reduced stomatal density and conductance. Therefore, ER is a prime candidate gene for studying the natural diversity of TE and photosynthesis in crops. Wheat is a major cereal crop in the world, and is cultivated in arid and semi-arid regions of the world, where water deficit and other environmental fluctuations limit its growth, development and yield. Since ER has been theorized to play a major role in plant development and TE for a number of species, this study investigates the multi-gene ER family in bread wheat and test (...truncated)