A Complex Nutrient Exchange Between a Gall-Forming Aphid and Its Plant Host

Abstract

It has been a long-standing question as to whether the interaction between gall-forming insects and their host plants is merely parasitic or whether it may also benefit the host. On its host Rhus chinensis, the aphid Schlechtendalia chinensis induces the formation of closed galls, referred to as horned galls. Typically, mature aphid populations comprise thousands of individuals, which is sufficient to cause the accumulation of high CO 2 levels in galls (on average 8-fold higher and up to 16 times than atmospheric levels). Large aphid populations also excrete significant amounts of honeydew, a waste product high in sugars. Based on 13 C isotope tracing and genomic analyses, we showed that aphid-derived carbon found in CO 2 and honeydew was recycled in gall tissues via photosynthesis and glycometabolism. These results indicated that the aphid-gall system evolved in a manner that allowed nutrient recycling, where the gall provides nutrients to the growing aphid population, and in turn, aphid-derived carbon metabolites provide a resource for the growth of the gall. The metabolic efficiency of this self-circulating system indicates that the input needed from the host plant to maintain aphid population growth less than previously thought and possibly minimal. Aside from the recycling of nutrients, we also found that gall metabolites were transported to other parts of the host plant and is particularly beneficial for leaves growing adjacent to the gall. Taken together, galls in the S. chinensis-Rhus chinensis system are highly specialized structures that serve as a metabolic and nutrient exchange hub that benefits both the aphid and its host plant. As such, host plants provide both shelter and nutrients to protect and sustain aphid populations, and in return, aphid-derived metabolites are channeled back to the host plant and thus provide a certain degree of "metabolic compensation" for their caloric and structural needs.

Molecular and Histologic Adaptation of Horned Gall Induced by the Aphid Schlechtendalia chinensis (Pemphigidae)

“…For example, a significant number (12 ± 6.34) of galls with large size (86.69 ± 13.15 × 53.63 ± 12.74 mm) is exclusively localized on tiny rachis wings instead of being present on bigger leaves. A gall can carry tens of thousands of aphids, and green galls are strong candidates to perform photosynthesis [ 24 , 25 ]. To gain insight into these unique characteristics, we conducted comparative analyses of gene expression on the differences and similarities of metabolic pathways between galls and leaf tissues.…”

“…Due to the combination of photosynthesis and honeydew recycling, the S. chinensis – R. chinensis system is highly efficient. During the long period of coevolution between S. chinensis and R. chinensis , the horned gall has developed a complex nutrient exchange mechanism with its host plant via sophisticated metabolism [ 25 ].…”

A new species of aphid of the genus Nipponaphis (Hemiptera: Aphididae: Hormaphidinae) from China, inducing galls on the trunk of a witch-hazel (Hamamelidaceae)

“…It has been questioned whether the interaction between gall-forming insects and their host plants is merely parasitic or whether it also benefits the host (Chen et al 2020). Galls are special products of co-evolution between insects and host plants with unique ecological significance.…”

Structural and Nutritional Peculiarities Related to Lifespan Differences on Four Lopesia Induced Bivalve-Shaped Galls on the Single Super-Host Mimosa gemmulata

“…The gall lifespans depend on structural, cytological, and chemical traits on the host plant cells stimulated by the associated galling organisms (Mani, 1964;Oliveira et al, 2010Oliveira et al, , 2016Jorge et al, 2018;Ferreira et al, 2019;Chen et al, 2020). Any changes in the galling organism behavior may lead to the disruption of the gall life cycle (Rezende et al, 2019) and compromise gall developmental stages.…”