Why sink strength is a key determinant of drought tolerance in common bean

Abstract

Throughout development, plants are constantly shifting resource allocation between their different tissue types; roots, stems, leaves, fruits and seeds. This allows them to balance resource gain, optimize growth, and increase reproductive output. While plants with different life history strategies have evolved very different patterns of allocation (ie. perennials conserve resources for the next year while annuals put all available resources into the next generation), the overall goal of increasing fitness underlies their behaviors. Still, it is not well understood what determines resource allocation into reproductive structures, specifically seeds. It’s clear that carbon availability and developmental processes play a crucial role - flowers, fruits and seeds must be produced, but a priority of allocation towards these structures must also be established and maintained to ensure high reproductive output. Drought is a significant factor which can impact allocation processes and seed filling. This can be due to changes in resource availability, as drought commonly decreases photosynthesis. However, allocation processes themselves are known to be affected by drought via signaling, particularly through the phytohormone abscisic acid. This means that even when resources themselves do not limit allocation and growth potential, other processes such as resource uptake into or metabolism within growing tissues may be slowed. Allocation processes therefore may be halted under drought stress, ultimately leading to decreased growth and/or seed filling. However, the degree to which different species and even different genotypes of a single species are impacted by drought differs strongly, resulting in some plants being better able to maintain allocation processes under drought. Lines which achieve this are deemed to be drought-tolerant. What allows drought-tolerant genotypes to maintain allocation and seed filling under drought? We set out to answer this question using common bean (Phaseolus vulgaris), where drought-tolerant lines have been shown to maintain higher allocation rates. Our goal was to gain a better understanding of the physiological underpinnings which control differences in allocation between drought-tolerant and drought-sensitive common bean lines. To begin, we tested how allocation processes, generally, were affected in tolerant and sensitive lines. We wondered if allocation to seeds was impacted by drought, would allocation towards any sink tissue be interrupted by drought? We found that within a genotype, drought’s impacts to growth and allocation acted in a consistent way across different sink tissues, such as leaves and seeds. That is, genotypes which had leaf growth strongly depressed by drought also had seed growth strongly depressed. This was not shown to be tightly correlated with resource availability or water status within the plant. Conversely, genotypes which maintained a high growth rate in one sink tissue, retained higher growth in other sinks. Genotypes which achieved higher growth resulted in a faster maturation of seeds, effectively allowing these lines to avoid potentially worsening drought. To better understand the differences in allocation between drought sensitive and drought tolerant lines, we quantified allocation across the different tissues of a plant over reproductive development. We found that drought-tolerant common bean lines (1) allocated biomass to seeds earlier, (2) allocated a larger percentage of total biomass to seeds than drought-sensitive lines, allowing the tolerant lines to achieve the same absolute yield as the sensitive line even with less total biomass, and (3) did not alter their seed filling profile under water stress, meaning the developmental program of seed filling was not altered by drought. In contrast, the sensitive line did have different seed filling profile under well-watered and water stressed. This suggests that the sensitive line alters development under drought whereas the tolerant does not. We believe that maintenance of allocation and therefore growth in the drought-tolerant line is the direct result of maintaining what is known as ‘sink strength’. Sink strength is defined as the ability of a growing, sink tissue, to obtain resources for use within the sink. Many mechanisms are known to be involved in setting sink strength, including resource uptake via transporters, proton pump and enzyme levels and activity. Proton pumps work to establish gradients across the membrane to drive resource uptake via transporters, and enzymes are involved in the breakdown and metabolism of materials, allowing for their transport into and use within sinks. We found that differences in these processes between genotypes determined differences in allocation and growth rate. When common bean seeds were floated in growth media containing sugar, uptake rates and growth were genotype and condition specific, rather than related to the concentration of sugar in the growth medium. This points to the seed itself as the point of regulation driving differences in seed filling. What underlies differences in the drought-tolerant line and the drought-sensitive line may be related to drought sensitivity, particularly to the hormone mentioned above, abscisic acid (ABA). We found that the drought-tolerant lines did not change the seed filling profile, nor seed filling rate or acidification rates in in vitro assays when exposed to drought and ABA, respectively. The drought sensitive line however did change its seed filling profile, seed filling rate and acidification rate under drought. Therefore, we believe that tolerant lines may have impaired drought sensitivity. This is perhaps through a reduced ability to produce, sense or respond to ABA, or potentially ABA production or sensing is constitutively on. However this is achieved, reduced drought sensitivity results in plants which maintain allocating resources towards sinks, importantly seeds, under drought stress. This allows them to fill seeds faster and increase the percent of total biomass allocated to seeds, increasing yields under drought.