Whole plant acclimation responses by finger millet to low nitrogen stress

Abstract

The small grain cereal, finger millet (FM, Eleusine coracana L. Gaertn), is valued by subsistence farmers in India and East Africa as a low-input crop. It is reported by farmers to require no added nitrogen (N), or only residual N, to produce grain. Exact mechanisms underlying the acclimation responses of FM to low N are largely unknown, both above and below ground. In particular, the responses of FM roots and root hairs to N or any other nutrient have not previously been reported. Given its low N requirement, FM also provides a rare opportunity to study long-term responses to N starvation in a cereal species. The objective of this study was to survey the shoot and root morphometric responses of FM, including root hairs, to low N stress. Plants were grown in pails in a semi-hydroponic system on clay containing extremely low background N, supplemented with N or no N. To our surprise, plants grown without deliberately added N grew to maturity, looked relatively normal and produced healthy seed heads. Plants responded to the low N treatment by decreasing shoot, root, and seed head biomass. These declines under low N were associated with decreased shoot tiller number, crown root number, total crown root length and total lateral root length, but with no consistent changes in root hair traits. Changes in tiller and crown root number appeared to coordinate the above and below ground acclimation responses to N. We discuss the remarkable ability of FM to grow to maturity without deliberately added N. The results suggest that FM should be further explored to understand this trait. Our observations are consistent with indigenous knowledge from subsistence farmers in Africa and Asia, where it is reported that this crop can survive extreme environments.

Keywords: crown root; finger millet; grain; lateral root; nitrogen stress; root; root hair; shoot.

FIGURE 1

Guide to the FM root system and the semi-hydroponic field fertigation growth system used in this study. Diagram of a FM root network (A). Crown roots are the thick roots that initiate from the crown region at the base of the shoot. Lateral roots initiate from the crown roots and can subsequently branch. Root hairs are present on both crown roots (as shown) and lateral roots. The fertigation growth system employed in this study consisted of 22 L plastic pails, 28 cm in diameter, filled with an inert baked clay medium (Turface^® ; B). Plants were allowed to grow to maturity as shown (C). Irrigation hoses delivered the nutrient solution except for nitrogen which was added manually as described.

FIGURE 2

Finger millet shoot responses to low N at different growth stages. FM in 2012 at 7 weeks of growth (A) and at harvest (B). FM in 2013 at 7 weeks of growth (C) and at harvest (D). All pails were 28 cm in diameter.

FIGURE 3

Shoot and root responses of FM to nitrogen limitation, at harvest. Representative mature, intact plants harvested in 2013, provided with +N and -N treatments (A). The seed heads were pre-harvested. The white scale bar at the lower right represents a length of 25 cm. Representative mature, entire root networks harvested in 2012 grown under +N and -N treatments, left and right respectively (B). The black scale bar at the lower right represents a length of 10 cm.

FIGURE 4

Correlations between FM shoot and seed head biomass and root architecture traits at harvest across nitrogen treatments. Number of crown roots vs. tillers (A). Shoot fresh weight vs. total root length (B), shoot fresh weight vs. total crown root length (C), shoot fresh weight vs. number of crown roots (D), shoot fresh weight vs. calculated average crown root length (E), and shoot fresh weight vs. total lateral root length (F). Number of crown roots vs. total crown root length (G). Seed head dry weight vs. total root length (H), seed head dry weight vs. total crown root length (I), seed head dry weight vs. number of crown roots (J), seed head dry weight vs. calculated average crown root length (K), and seed head dry weight vs. total lateral root length (L). Pearson r values are displayed. A single asterisk denotes significance at P < 0.10. A double asterisk denotes significance at P < 0.05.

FIGURE 5

Root hair morphometric traits from 2013 plants at harvest. In 2013 and 2012 (data in Supplemental Figure S1), four different classes of crown roots were sampled based on their lengths/ages (A), and then examined for root hairs at five different segments spaced evenly along each crown root using light microscopy with 5x magnification (B). Root hairs were quantified for length (C) and density (D) at different segments of the crown roots (x-axis) ranging from the top/nearest the shoot (crown root segment 1) to near the root tip (crown root segment 5). A blue asterisk (^∗) directly above a mean data point denotes a significant difference in the root hair trait (at P < 0.05) between N treatments within an individual crown root segment. An asterisk above the green dashed line denotes a significant difference in the root hair trait (at P < 0.05) between the top crown root segment (segment 1) and the bottom crown root segment (segment 2) within the +N treatment (red asterisk) or the -N treatment (black asterisk). All statistical analyses were performed with unpaired t-tests (with Welch’s correction where unequal variances required).

FIGURE 6

Summary of the effects of low N stress on FM architecture. Low N resulted in a reduction in end-season shoot biomass and seed head biomass associated with fewer tillers compared to plants receiving higher N (A). Fewer crown roots were initiated in 2013 in response to the -N treatment (B), likely responsible for the reduction in total lateral root system length (C). The calculated average crown root length was unchanged between nitrogen treatments. No consistent changes in root hair length or density occurred for root hairs along the crown roots in response to the -N treatment (D). However, in both N treatments, root hairs were generally longer and denser at the top of the crown roots than at the bottom of the crown roots (D).