Stem-borne roots as a framework to study trans-organogenesis and uncover fundamental insights in developmental biology.

Plants have a remarkable ability to generate organs with a different identity to the parent organ, called 'trans-organogenesis'. An example of trans-organogenesis is the formation of roots from stems (a type of adventitious root), which is the first type of root that arose during plant evolution. Despite being ancestral, stem-borne roots are often contextualised through lateral root research, implying that lateral roots precede adventitious roots. In this review we challenge that idea, highlight what is known about stem-borne root development across the plant kingdom, the remarkable diversity in form and function, and the many remaining evolutionary questions. Exploring stem-borne root evolutionary development can enhance our understanding of developmental decision making and the processes by which cells acquire their fates.

Root submergence enhances respiration and sugar accumulation in the stem of flooded tomato plants.

Flooding is a major environmental constraint that obliges plants to adopt plastic responses in order to cope with it. When partially submerged, tomato plants undergo profound changes involving rearrangements in their morphology and metabolism. In this work, we observed that partial submergence markedly dampens root respiration and halts root growth. However, the flooded hypocotyl surprisingly enhances oxygen consumption. Previous results demonstrated that aerenchyma formation in the submerged tomato stem re-establishes internal oxygen tension, making aerobic respiration possible. Indeed, potassium cyanide abruptly stops oxygen uptake, indicating that the cytochrome c pathway is likely to be engaged. Furthermore, we found out that leaf-derived sugars accumulate in large amounts in hypocotyls of flooded plants. Girdling and feeding experiments point to sucrose as the main carbon source for respiration. Consistently, submerged hypocotyls are characterized by high sucrose synthase activity, indicating that sucrose is cleaved and channelled into respiration. Since inhibition of hypocotyl respiration significantly prevents sugar build-up, it is suggested that a high respiration rate is required for sucrose unloading from phloem. As substrate availability increases, respiration is fuelled even more, leading to a maintained allocation of sugars to flooded hypocotyls.

Maintenance of photosynthetic capacity in flooded tomato plants with reduced ethylene sensitivity.

Ethylene is considered one of the most important plant hormones orchestrating plant responses to flooding stress. However, ethylene may induce deleterious effects on plants, especially when produced at high rates in response to stress. In this paper, we explored the effect of attenuated ethylene sensitivity in the Never ripe (Nr) mutant on leaf photosynthetic capacity of flooded tomato plants. We found out that reduced ethylene perception in Nr plants was associated with a more efficient photochemical and non-photochemical radiative energy dissipation capability in response to flooding. The data correlated with the retention of chlorophyll and carotenoids content in flooded Nr leaves. Moreover, leaf area and specific leaf area were higher in Nr, indicating that ethylene would exert a negative role in leaf growth and expansion under flooded conditions. Although stomatal conductance was hampered in flooded Nr plants, carboxylation activity was not affected by flooding in the mutant, suggesting that ethylene is responsible for inducing non-stomatal limitations to photosynthetic CO2 uptake. Upregulation of several cysteine protease genes and high protease activity led to Rubisco protein loss in response to ethylene under flooding. Reduction of Rubisco content would, at least in part, account for the reduction of its carboxylation efficiency in response to ethylene in flooded plants. Therefore, besides its role as a trigger of many adaptive responses, perception of ethylene entails limitations in light and dark photosynthetic reactions by speeding up the senescence process that leads to a progressive disassembly of the photosynthetic machinery in leaves of flooded tomato plants.

Tomato fruit development in the auxin-resistant dgt mutant is induced by pollination but not by auxin treatment.

In tomato (Solanum lycopersicum Mill.), auxin is believed to play a pivotal role in controlling fruit-set and early ovary growth. In this paper we investigated the effect of the reduced auxin sensitivity exhibited by the diageotropica (dgt) tomato mutant on ovary growth during early stage of fruit development. Here we show that in hand-pollinated ovaries fruit-set was not affected by the dgt lesion while fruit growth was reduced. This reduction was associated with a smaller cell size of mesocarp cells, with a lower mean C values and with a lower gene expression of the expansin gene LeExp2. When a synthetic auxin (4-CPA, chlorophenoxyacetic acid) was applied to the flowers of wild type plants, parthenocarpic ovary growth was induced. On the contrary, auxin application to the flowers of dgt plants failed to induce parthenocarpy. Hand-pollinated ovaries of dgt contained higher levels of IAA compared to wild type and this was not associated with high transcript levels of genes encoding a key regulatory enzyme of IAA biosynthesis (ToFZYs) but with lower expression levels of GH3, a gene involved in the conjugation of IAA to amino acids. The expression of diverse Aux/IAA genes and SAUR (small auxin up-regulated RNA) was also altered in the dgt ovaries. The dgt lesion does not seem to affect specific Aux/IAA genes in terms of transcript occurrence but rather in terms of relative levels of expression. Transcript levels of Aux/IAA genes were up regulated in auxin-treated ovaries of wild-type but not in dgt. Together, our results suggest that dgt ovary cells are not able to sense and/or transduce the external auxin signal, whereas pollinated dgt ovary cells are able to detect the IAA present in fertilized ovules promoting fruit development.

Hormonal interplay during adventitious root formation in flooded tomato plants.

Soil flooding, which results in a decline in the availability of oxygen to submerged organs, negatively affects the growth and productivity of most crops. Although tomato (Solanum lycopersicum) is known for its sensitivity to waterlogging, its ability to produce adventitious roots (ARs) increases plant survival when the level of oxygen is decreased in the root zone. Ethylene entrapment by water may represent the first warning signal to the plant indicating waterlogging. We found that treatment with the ethylene biosynthesis inhibitor aminoethoxyvinylglycine (AVG) and the auxin transport inhibitor 1-naphthylphthalamic acid (NPA) resulted in a reduction of AR formation in waterlogged plants. We observed that ethylene, perceived by the Never Ripe receptor, stimulated auxin transport. In a process requiring the Diageotropica gene, auxin accumulation in the stem triggered additional ethylene synthesis, which further stimulated a flux of auxin towards to the flooded parts of the plant. Auxin accumulation in the base of the plant induces growth of pre-formed root initials. This response of tomato plants results in a new root system that is capable of replacing the original one when it has been damaged by submergence.