Efficient nitrogen allocation and reallocation into the ear in relation to the superior vascular system in low-nitrogen tolerant maize hybrid

Highlights

• N-efficient cultivar developed more and heavier grains under low-N stress.

• N-efficient cultivar allocated more soil-derived N to the ear before silking.

• N-efficient cultivar reallocated more vegetative-N to the ear after silking.

• Less N was allocated to and more N was reallocated from the lower leaves and stem.

• A superior vascular system contributed to efficient N allocation and reallocation.

Abstract

Efficient nitrogen (N) utilization is crucial for maintaining grain yield under low N input. Less is known about the role of within-plant N allocation and reallocation on ear development and the factors determining N allocation during the critical period around silking. In this study, two maize hybrids, ZD958 (N-efficient) and LY99 (N-inefficient), were evaluated in a 2-year field experiment under two N rates (60 and 180 kg N ha^-1). N transport and allocation into the ear during critical period were investigated using ¹⁵N stable isotopic tracer. The number and area of vascular bundles in ear shank, above- and below-ear internode were measured. The two hybrids did not differ in grain yields under high N rate. However, the grain yield of ZD958 was 43.6% higher than that of LY99 under low N rate, deriving from 26.3% and 13.9% increment in grain number and grain weight, respectively. At early critical growth stage before silking, ZD958 increased allocation of soil-derived N to the ear by 225.2% compared with LY99 under low N rate. At late critical growth stage after silking, ZD958 increased allocation of soil-derived N and reallocation of vegetative-N to the ear by 45.5% and 116.6%, respectively, compared with LY99 under low N rate. As a result, ear growth rate and ear N content of ZD958 was 22.2% and 69.1% higher than that of LY99 at the end of critical period. During N allocation and N reallocation, the lower leaves were sacrificed and the N status of the ear leaf and upper leaves was mostly maintained to sustain photosynthesis. In the ear shank, flux rate and N concentration of the xylem sap in ZD958 were 53.1% and 32.5% greater at silking stage, and were 40.8% and 27.5% greater at 14-days after silking, respectively, compared with LY99 under low N rate. Correspondingly, the number and average area of big vascular bundles in ear shank of ZD958 were 56.2% and 31.0% greater compared with LY99. Parameters characterizing the number and area of big vascular bundles were positively correlated with N allocation and grain yield, while that of small vascular bundles were negative. It is concluded that efficient N allocation to the ear at critical period is essential for ear growth and the subsequent vegetative-N remobilization, so as to improve low-N tolerance in high-yielding maize hybrids. A superior vascular system around the ear, especially in the ear shank, can enhance N allocation into the ear and could be regarded as a physiological selection trait in maize breeding to improve nitrogen use efficiency.

Introduction

Maize (Zea mays L.) is an important staple crop in the world. In 2021, maize production accounts for 42.2% of the total cereal production in China (OECD/FAO, 2021). Maize productivity heavily depends on nitrogen (N) fertilizer input (Chen et al., 2011, Ciampitti and Vyn, 2012, Arisede et al., 2020). However, farmers frequently overuse N fertilizer to guarantee maize yield (Cui et al., 2010, Hou et al., 2012, Hou et al., 2020, Kumar et al., 2019, Liao et al., 2012). Excess N fertilizer input results in resource waste and environmental pollution, such as eutrophication (Bacenetti et al., 2016), greenhouse gas emissions (Chen et al., 2014a, Mateo-Marín et al., 2020), and soil acidification (Raza et al., 2020, Hao et al., 2022). Cultivating N-efficient maize varieties is demonstrated to be a feasible strategy to reduce N fertilizer input while maintaining a reasonable yield (Dwyer et al., 1995, Ciampitti and Vyn, 2012, Chen et al., 1999, Mi et al., 2007, Mueller et al., 2019, Li et al., 2019, Li et al., 2001).

Under limited N supply, allocation and reallocation of N within plant play crucial roles in plant growth (Jeschke and Pate, 1991a and 1991b; Ta and Weiland, 1992; Hirel et al., 2001; Gallais et al., 2006). In maize, it is found that N transport in the xylem and N recycling in the phloem are greater in the N-efficient varieties (Chen et al., 2014a, Liu et al., 2019). During grain filling stage, N in the vegetative organs is remobilized and reallocated to the grains for protein synthesis (Pommel et al., 2006, Drouet and Bonhomme, 1999, Mi et al., 2016). Recent molecular studies in rice indicate that the transport proteins OsLHT1, OsNPF7.3 and OsLSD1.1 are located in the vascular bundles and are responsible in the reallocation of N from vegetative organs to panicle and grains (Fang et al., 2017, Guo et al., 2020, Xu et al., 2017). In maize, the vascular system in the stem around ear node and in the ear shank controls nutrient transport between the vegetative organs and the ear, therefore may play a crucial role in N allocation and reallocation (Shane et al., 2000, Piao et al., 2016, Yang et al., 2021, Ren et al., 2020). In general, more vascular bundles and larger bundle areas are beneficial to N transportation (Travaglia et al., 2012, Ren et al., 2020). Nevertheless, less is known about the relationship between maize vascular system, N allocation and reallocation, and N use efficiency (NUE).

Genetic improvement increases maize productivity largely by enhancing biomass production and N accumulation (Buckler et al., 2006; Lynch, 2013; Ma et al., 2014; Mi et al., 2016). Current maize hybrids are characteristic of high N-uptake efficiency and high stay-green degree under intensive agriculture (Tollenaar and Lee, 2002, Badu‐Apraku et al., 2015). The importance of N allocation and reallocation within plant is largely ignored. The four weeks bracketing silking stage is regarded as the critical period determining grain number per ear and potential grain weight (Mueller et al., 2019, Li et al., 2001). During this period, the growth and development of young ear are sensitive to N deficiency (Chen et al., 2014b, Seebauer et al., 2004, Yin et al., 2003). Limited N supply decreases grain number per ear and potential grain weight by inhibiting floret primordia development and endosperm cell division, ultimately decreasing size and strength of sink (Andrade et al., 2002, Donnison et al., 2007, Mueller et al., 2019, Nasielski and Deen, 2019, Van Zwieten et al., 2010, Pico et al., 2021). Sink size and sink strength would have subsequent effect on N reallocation from the vegetative organs. So, we hypothesize that, under limited N supply, it should be crucial to allocate relatively more soil-derived N to ear at pre-silking stage to develop more fertile florets (potential grains), and then reallocate more vegetative-N to the ear at post-silking stage to ensure grain development (Kant et al., 2011, Guo et al., 2015, Juraniec et al., 2017, Ning et al., 2017).

Previously we identified the genotypic difference in within-plant N remobilization between N-efficient and N-inefficient maize hybrid (Liu et al., 2021b). In this research, we further investigate the underlined mechanism by checking the following hypotheses: a) N-efficient maize hybrid is efficient in soil-derived N allocation and vegetative-N reallocation; b) N-efficient maize hybrid allocates less N to and reallocates more N from lower leaves and stem, to coordinate ear growth and photosynthesis, c) a superior vascular system in the shank and internode promotes N transport and therefore contributes to efficient N allocation and reallocation.